Monkeys

Question 1

What are the families of new world and old world monkeys?

What species are in each family?

Answer 1

• Overview (F8):
  
  • Over 270 species of monkeys (see table 37-1 for monkey species)
  • New world monkeys
    
    • Cebidae (capuchin, squirrel, callitrichids)
      
      • Subfamily Callitrichinae (smallest monkeys)
    • Aotidae (owl monkey)
    • Pitheciidae (saki monkeys)
    • Atelidae (howler, spider, woolly monkeys)
  • Old world monkeys
    
    • Catarrhini parvorder
      
      • Family Cercopithecidae (macaques, baboons, guenons, mangabeys, vervets, drills,
        
        • Subfamily Cobolinae – langurs, colobus

Question 2

Describe the unique anatomical characteristics of monkeys.

What is the largest monkey species?

Which group has ischial callosities?

What species display dramatic sexual dimorphism?

What is unique about howler monkey laryngeal anatomy?

How do the fermentation strategies of colobinae & howler monkeys differ?

Answer 2

• Unique anatomy
  
  • Similar features to humans
    
    • Fingerprints
    • Convergent eye sockets (binocular vision)
    • Rods and cones for color vision
    • Retinal fovea for sharp visual image
    • Grasping hands
    • Large brains
    • Clavicles
    • 2 pectoral mammary glands
  • Dental formula
    
    • Old world: 2/2:1/1:2/2:3/3
    • New world: 2/2:1/1:3/3:3/3 (except Callithrix, Leontopithecus, Sanguinus, Cebus)
  • Prehensile tails only in some new world species
  • Prehensile thumbs in old world monkeys, except colobus
  • Mandrill is the largest monkey species
  • Ischial callosities (Cercopithecines)
  • Dramatic sexual dimorphism
    
    • Males > females in baboons
    • Male lion-tailed macaques have flamboyant gray mane
    • Male proboscis monkeys have an enlarged nose
  • Howler monkeys have large hyoid bones for vocalization
  • Larygneal diverticula (air sacs) are present in most monkeys, and many OW species have cheek pouches as well (to store food)
  • Folivorous species
    
    • OW Colobinae subfamily (colobus, langurs, proboscis)
      
      • Sacculated stomach for foregut fermentation
    • NW howler monkeys use hindgut fermentation in the cecum and colon
    • Antibiotic use in these species may cause dysbiosis, and transfaunation may be necessary

Question 3

What are the differences between new world and old work monkeys?

Nose

Tails

Digits

Sexual Intumescences & Sex Skin

Scent Glands

Cheek Pouches

Air Sacs

Lungs

Answer 3

Question 4

Describe the reproductive anatomy & physiology of monkeys.

Do males provide parental care?

What group has reproductive suppression?

Which group of monkeys has a menstrual cycle?

What is sex skin? Which monkeys display it?

Do males have an os penis?

What is the uterus and placentation anatomy?

Which group of monkeys has higher endogenous sex hormones? How does this affect contraception?

Answer 4

• Reproduction (F8):
  
  • Males generally do not provide parental care, except in callitrichids
    
    • Callitrichids have female reproductive suppression in family groups, with only the dominant female being reproductively active
  • Monkeys have long period or parental dependency
  • Both OW and NW monkeys have and estrous cycle, but only OW monkeys have a menstrual cycle
  • Most monkeys are reproductive year round (except Japanese macaques which are more seasonal)
  • Many OW monkeys have ‘sex skin’ or cyclic perineal hyperemia and tumescence during ovulation/elevated estrogen
  • Males have an os penis
  • Most species have lactational anestrus
  • Females have simplex uterus and hemochorial placentation
    
    • Callitrichids exhibit chorionic placental fusion of fraternal twins with blood chimerism
  • For contraception, NW monkeys have higher endogenous sex steroids and require higher MGA doses than other primates

Question 5

How do human cultivated fruits and vegetables differ from those in the wild? How does this affect nonhumn primate diets?

What is the cause of simian bone disease (rickets)?

What group of primates require dietary vitamin D3?

What is a common sign of vitamin C deficiency in squirrel monkeys?

Which monkeys have follivorous diets? How does their GI anatomy change? What diesease are they predisposed to?

Answer 5

• Nutrition and diet
  
  • Ingest 2-6% of BW per day
    
    • Human fruits/vegetables are lower in protein, fiber, and calcium, and higher in sugar than what monkeys would find in the wild
    • Feed no more than 30% of dry matter as produce
    • Feed 70% produce + 30% biscuits OR 50% produce + 50% canned food
  • Nonhuman primates 7-10% protein requirement (up to 12.5% in pregnant females)
  • Simian bone disease (rickets)
    
    • Dietary Ca deficiency
    • New world monkeys require pre-formed dietary vitamin D3 (cholecalciferol)
      
      • Sunlight is also important for UVB
      • Marmosets have the highest vitamin D3 requirement
  • All primates have a requirement for vitamin C (deficiency is ‘scurvy’)
    
    • Cephalohematoma is most common sign in young squirrel monkeys
• Folivorous diet
  
  • Trachypithecus, Semnopithecus, Presbytis, Colobus have sacculated stomachs with two bands of longitudinal teniae
  • High fiber requirement
  • Frequent feeding to promote fermentation
  • Colobus can develop gluten-intolerant enteropathy if fed wheat, barley, rye diets
  • Browse high in lignin or indigestible fibers that cannot be broken down by microflora and predisposes to phytobezoars

Question 6

Describe an ideal preventative medicine strategy for monkeys.

What vaccines do they need?

Describe TB testing.

Answer 6

1. Preventative medicine
   
   1. Vaccination – tetanus (toxoid), rabies (killed), less commonly measles (avoid modified-live)
   2. Routine fecal screening
   3. 31 day quarantine periods (monkeys receive 3 TB tests at 14 day intervals, with the final reading at 72 hours after the last test)

Question 7

Describe the physical restraint of monkeys.

What techniques and tools are used?

How can training facilitate anesthetic induction?

Answer 7

Physical Restraint

• Variety of methods - nets, squeeze cages, head-lock devices
• Any restraint is stressful - minimize duration, also increased risk of bites (and zoonotic disease transmission) - use leather gloves and/or towels
• Hoop nets useful for species ≤ 4 kg
• Manual restraint excellent for small species (tamarins, marmosets)
  
  • Hoop net  lock head w/ thumb + index finger, upper body w/ other 3 fingers and hindlimbs with other hand
    
    • Suitable for minor procedures (wound Tx, injections, venipuncture)
• Squeeze cages typical for animals too dangerous to handle by hand

Psychological Restraint (Taming)

• Many primates will accept IM injections or IV injection/blood collection via positive reinforcement/operant conditioning

Question 8

Describe the vascular access sites for monkeys.

Answer 8

Vascular Access

• Femoral vein - approach just distal to inguinal canal
  
  • Lies caudal to femoral artery, just under the skin in triangle formed by abdominal, sartorius and pectineus muscles
• Saphenous (popliteal) vein - can be used for IV catheter (even in callitrichids)
• Less commonly jugular vein, cephalic veins
• If tail - lateral coccygeal veins - at dorsolateral surface of base of tail

Question 9

Describe the intubation of monkeys.

What positioning can facilitate intubation?

What are some common problems with intubation? How can they be addressed?

Answer 9

Endotracheal Intubation

• Readily achieved in most species w/ laryngoscope and appropriate sized tube
• Position - dorsal recumbency on table w/ head flexed slightly backwards or sitting position w/ head flexed backwards
• Topical anesthetic on larynx will reduce laryngospasm (can dilute lidocaine, don’t go > 4 mg/kg)
• Relatively short tracheas with bifurcation close to neck
  
  • Easy to intubate a mainstem bronchus and ventilate one lung only
  • Prevent by premeasuring tube to base of neck prior to placement
• If smaller than squirrel monkey - can use urinary catheter or infant feeding tube as ET tube
• Squirrel monkey size - uncuffed 2-2.5 ET tube
• Most other spp. b/w 1-20 kg  3-5 mm cuffed ET tube

Question 10

Describe the anesthetic strategies for monkeys.

What oral meds can be offered?

What are some common issues with darting monkeys?

What are typical reocmmended protocols?

Answer 10

Sedation and General Anesthesia

Oral Administration of Drugs

• Ingestion of full dose is voluntary action, depends primarily on palatability, person offering, if food has visibly been altered, etc.  unpredictable absorption
• Bioavailability and absorption time vary depending on if absorbed via oral mucosa or intestine
  
  • If swallowed - 1^st pass metabolism may have sig. effect on lowering effective drug conc.
• No reports of oral admin as a consistent, safe and reliable method

Parenteral Anesthesia

• Via hand injection or projectile dart
  
  • Darting fast, effective but w/ sig. disadvantages (stress, pain, trauma)
    
    • Relatively small target areas - can be difficult to hit, esp. in moving animals
    • Target - usually hip/thigh, rarely in triceps or shoulder of larger primates
• Most recommendations include a dissociative anesthetic alone or in combo w/ α2-adrenoceptor agonist or benzodiazepine
• Common to combine 2+ drugs  minimize volume, increase potency, stable safe plane w/ adequate muscle relaxation/analgesia, improve recovery quality/time, minimize side effects

Inhalation Anesthesia

• Alone or used to maintain anesthesia after induction
• Isoflurane (MAC 1.2%) and sevoflurane (MAC 2%) most common; halothane (MAC 0.9%)
• Small primates can be restrained for facemask or induction chamber
• Clear advantage - reversibility, use of oxygen as carrier (normally ensures adequate O2)
• Expected to cause dose-related CV and resp depression

Suggested Protocols

• ≤ 4 kg - manual restraint for inhalation anesthesia OR 0.02-0.05 mg/kg Med + 5-8 mg/kg K IM
• ≥ 4 kg - 5-8 mg/kg K + 0.02-0.05 mg/kg Med IM
• Most duration 30-45 minutes, but may awaken suddenly
• Spray epiglottis w/ lidocaine, intubate and provide w/ supp. O2
• Inhalation (isoflurane) excellent for maintenance
• Keep separate, caged, and unable to climb until fully recovered

Question 11

What are some of the most common disorders of vitamin D and calcium metabolism in monkeys?

Describe the pathophysiology of secondary hyperparathyroidism.

What about renal secondary hyperparathyroidism?

What clinical signs does this lead to in monkeys?

What groups of monkeys are particularly susceptible?

Answer 11

Disorders of Vitamin D and Ca/Phos Metabolism

1. Secondary hyperparathyroidism - decreased Ca or excess P
   
   1. Hypocalcemia - increased PTH secretion → increased bone resorption → bone replaced by fibrous connective tissue
   2. Leads to distorted limbs, kyphosis, long bone fx, thickening of maxillary/mandible (fibrous osteodystrophY)
2. Renal secondary hyperPTH - secondary to chronic renal failure: dec GFR → P retention, dec Ca
   
   1. Kidney damage can also inhibit vit D activation (kidney responsible for 25-OH-vit D to 1,25-OH-vit D step
3. Rickets - failure to mineralize osteoid, immature animals before epiphyseal closure
4. Osteomalacia - failure to mineralize osteoid - mature animals; see folding fractures of ribs and long bones
5. Fibrous osteodystrophy - calvarium, maxilla and mandibles swollen; teeth loosely attached/shed
6. NWM more common for rickets/osteomalacia but can happen in young OWM and apes - animals housed indoors, no full spectrum light
   
   1. NWM require higher vit D in diets than OWM

Question 12

Vitamin C is an essential nutrient of all NHP except for what group?

What are the clincial signs of scurvy?

Is there a pathognomonic lesion? What species does this occur in?

What are the clinical signs of hypovitaminosis E? What species appear to be particularly susceptible?

Answer 12

Hypovitaminosis C

1. Vitamin C is an essential nutrient in all NHP except in strepsirrhines (lemurs, lorises, bush babies)
2. Scurvy - decreased collagen stability, see gingival bleeding, gingivitis, loosening of teeth, petecchiation, periarticular/subperiosteal hemorrhage
3. Cephalohematomas - pathognomonic in squirrel monkeys
4. Anemia - secondary to role of ascorbic acid in Fe absorption and folic acid

Hypovitaminosis E

1. Hemolytic anemia and necrotizing myopathy in owl monkeys, marmosets, gelada baboons – responds with vitamin E supplementation
   
   1. Owl monkeys, capuchin monkeys, and callitrichids have particularly high requirements

Question 13

What group of monkeys is particularly prone to hemosiderosis?

How is this difinitively diagnosed on histopathology?

Answer 13

Hemosiderosis

1. One of the most common findings of managed callitrichids
2. PRUSSIAN BLUE histo stain; brown-yellow granular material on H/E
3. Ferrous (Fe2+) iron in Kupffer cells, hepatocytes
4. Due to excessive intake + inc enterocyte absorption
5. Liver enzymes usually normal
6. Brown discoloration of liver
   
   1. In golden lion tamerins, ddx Dubin-Johnson-like disease on regular staining because hyperbilirubinemia also appears as green-brown granular/globular pigment on histo

Question 14

What are three common metabolic diseases of monkeys?

Which type of diabetes is most common? What are the clinical signs? How does the pancreas appear on histopathology?

What species are particulary susceptible to hepatic lipidosis?

What species are susceptible to amyloidosis ? What sites is amyloid commonly deposited in? How is amyloid deposition confirmed histologically?

Answer 14

Diabetes mellitus - type 1 and 2

1. T2 most common (associated w/ obesity) - both OWM and NWM
2. CS - polyphagia, PU/PD
3. Islet cells replaced by amyloid (homogenous extracellular eosinophilic material) - apple green (Congo red stain) birefringence under polarized light

Nutritional fatal fasting syndrome (fatal fatty liver syndrome)

1. Obese female macaques
2. Acute disorder - anorexia, depression, large weight loss - see azotemia (renal tubular lipidosis), yellow/tan hepatomegaly

Amyloidosis

1. Most common secondary reactive amyloidosis - aged macaques, common marmosets, baboons
2. Amyloid A deposition - liver, spleen, adrenal glands, intestine
3. Macaques - associated with chronic enterocolitis, diarrhea
4. In liver - process starts in space of Disse (perisinusoidal space)
   
   1. In intestines - starts in lamina propria

Question 15

Describe the inflammatory diseases of monkeys.

What are the clinical signs of wasting marmoset syndrome? What lesions are associated with this disease on necropsy? What nutritional support may be useful in these cases?

What species are predisposed to chronic colitis? What type of histologic lesions are typically present?

What is “sprue” in colobus monkeys? What dietary modifications have made this disease less common?

Answer 15

Inflammatory Diseases

Wasting marmoset syndrome

1. Severe weight loss, generalized weakness, muscle atrophy, intermittent/chronic diarrhea, anemia, alopecia, paraplegia
2. Associated w/ chronic lymphocytic enteritis, inflammatory bowel disease, CKD with tubulointerstitial nephritis and glomerulopathy resulting in severe maldigestion/malabsorption
3. Unknown etiology
4. Syndrome may be improved when protein inc to 24% in pellets

Chronic colitis

1. Managed macaques and baboons
2. Recurring enteric infections, dysbiosis, dysregulation of mucosal defenses, environmental stress, +/- dietary hypersensitivities
3. Cecum and ascending colon most severely affected – lymphoplasmacytic colitis with crypt abscesses and ocassional ulceration

Colobus ‘sprue’

1. Diarrhea, hypoproteinemia → effusion, edema including colonic mural edema
2. Less common now with biscuits that have been modified to have more fiber and protein and less cereal

Question 16

Describe the inflammatory diseases of monkeys.

What species are particulary susceptible to cystic livers? How does this affect them?

What is endometriosis? How common is it? What species are particulary susceptible?

Answer 16

Cystic liver

1. Cotton top tamarins
2. Subclinical, similar to polycystic liver disease in humans, cysts originate from intrahepatic bile ducts

Endometriosis

1. Ectopic endometrial tissue
2. Most common repro disorder of menstruating OWM
3. Incidence increases w/ age +/- genetic predisposition
4. Rhesus and cynomolgus macaques
5. Single to multiple soft red/brown masses on serosal/peritoneal surfaces - cysts filled w/ brown fluid (‘chocolate cysts’); commonly intraabdominal but may be extraperitoneal (liver, lungs)Infertility frequent

Question 17

What are two common neoplasias of callitrichids?

Answer 17

Neoplastic Diseases

1. Colonic adenocarcinoma - cotton top tamarins - diarrhea, weight loss, intestinal obstruction; predisposed if repeated colitis; not seen in free ranging animals
2. Intestinal adenocarcinomas - marmosets - duodenum/jejunum junction - napkin ring constriction; common in aging marmosets

Question 18

What is the etiologic of Herpes B?

What species are the natural host?

Mortalities have been observed in which species? Which species has had persistent nonclinical infections?

How is this diseaase transmitted? How is virus shed?

What are typical clinical signs in macaques? What about in other species?

Is it zoonotic?

Answer 18

1. Macacine herpesvirus 1 aka Herpesvirus simiae aka Herpes B virus
   
   1. Eosinophilic intranuclear inclusion - enzootic in Asian macaques
   2. Latent in trigeminal + lumbosacral ganglia
   3. Intermittent reactivation + shedding during stress
   4. Shed in oral + genital secretions, vesicle fluid
   5. Transmission - bites, scratches, venereal
   6. CS in macaques- vesicles and ulcers on oral mucosa, lips, conjunctiva
   7. Aberrant species - fatal - owl monkeys, marmosets, African green monkeys, Barbary macaques, bonnet monkeys, gibbons, DeBrazzas
      
      1. Asymptomatic interspecies transmission in capuchins housed with macaques
   8. Zoonotic - lethal encephalomyelitis

Question 19

Besides herpes B, what are the other alphaherpesviruses that affect monkeys?

What are the etiologic agents of herpes simplex?

• What are the clinical differences of infection with human herpes simplex viruses in old world and new world primates?

What is the etiologic agent of herpesvirus papio 2?

• What is the natural host and how do lesions appear in that species?
• What other species are susceptible and how do they present?

What is the etiologic agent of herpesvirus tamarinus?

• What is the natural host and how do lesions appear in that species?
• What other species are susceptible and how do they present?

What is the etiologic agent of simian varicella?

• What groups of monkeys are susceptible?
• What clinical signs and lesions are common with this virus?

Answer 19

1. Human herpes simplex 1 and 2 (HHV-1, HHV-2)
   
   1. Mild localized mucocutaneous lesions OWM; NWM highly susceptible (marmosets, tamarins) fatal encephalitis
   2. Human to monkey, monkey to monkey
   3. Oral, lingual, genital vesicles/ulcers → necrotizing meningoencephalitis
2. Simian varicella virus (Cercopithecine herpesvirus - 9)
   
   1. Erythematous disease OWM
   2. Transmission - respiratory
   3. CS - diffuse inguinal rash that spreads centripetally → vesiculoulcerative dermatitis trunk/face/extremities; pruritus; may disseminate to internal organs if immunosuppressed; papule → vesicle → crust
   4. DDx B virus (mucocutaneous) and morbillivirus (not vesicular

Question 20

What betaherpesviruses infect primates?

what are the clinical signs? What animals are more likely to be infected? What are the classic inclusion bodies?

Answer 20

Betaherpesviruses

1. Simian cytomegaloviruses
   
   1. Basophilic intranuclear “owl’s eye” inclusions in pneumoyctes - NWM and OWM
   2. Normal mature host - asymptomatic
   3. CMV common in immunosuppressed SIV or SRV macaques; if reactivated - necrotizing meningitis, neuritis, enterocolitis, interstitial pneumonia; hyperemic plaques in intestine
   4. NOT zoonotic

Question 21

What are the gammaherpesviruses that affect monkeys? What is their tropism?

What is the etiologic agent of rhesus lymphocryptovirus?

• What human virus is this related to?
• What species are affected?
• What are the lesions? What is the animal is immunosuppresed?

What is the etiologic agent of marmoset lymphocryptovirus?

• What species are affected?
• How common is this?
• What are the typical lesions

What is the etiologic agent of herpesvirus saimiri?

• What is the natural host?
• What other species are susceptible?
• What lesions occur as a result of infection?

What is the etiologic agent of rhesus rhadinovirus?

• What species is affected?
• What are the lesions that occur?

What is the etiologic agent of herpesvirus ateles?

• What is the natural host?
• What other species are susceptible?
• How do lesions differ across species?

Answer 21

Gammaherpesviruses

1. Rhesus lymphocryptovirus (RhLCV, Macacine herpesvirus 4) - OWM, NWM
   
   1. Related to human herpesvirus 4 (Epstein-Barr)
   2. Epizootic
   3. If immunodeficient - SIV rhesus macaques - may progress to lymphoma (B cell most common)
   4. Oral hairy leukoplakia - oral mucosa/esophagus - prolierative epidermal lesion
   5. NOT zoonotic
2. Callitrichine herpesvirus 3 (marmoset lymphocryptovirus)
   
   1. Related to RhLCV - B cell lymphoma of GIT and LN
   2. NOT zoonotic
3. Herpesvirus saimiri (Saimiriine herpesvirus 2)
   
   1. T lymphotropic
   2. Enzootic in squirrel monkeys
   3. Transmission to tamarins, owl monkeys, marmosets - acute lymphoproliferative disorder w/ splenomegaly, peripheral/visceral lymphadenomegaly
   4. CD3 and CD8 positive T lymphs
   5. May see natural transmission in zoo managed callitrichids - DON’T HOUSE SQUIRREL MONKEYS WITH MARMOSETS/TAMARINS
   6. NOT zoonotic
4. Rhesus rhadinovirus (RRV, Macacine herpesvirus 5)
   
   1. Related to retroperitoneal fibromatosis-associated herpesvirus (RFH)
   2. RRV - Rhesus macaques, asymptomatic, infection early in life
   3. RFHV - associated w/ simian retrovirus infections, leads to mesenchymal neoplasia - retroperitoneal or subcutaneous fibromatosis
      
      1. Multiple firm pale masses in peritoneum or SC/myofascial planes

Question 22

Describe the poxviruses that affect monkeys.

Monkeypox

• What species are susceptible to monkeypox infections? What species have axymptomatic infecitons? Is it zoonotic?
• What are teh two clades?
• How is it transmitted?
• What are the clinical signs and lesions?

Cowpox

• Cowpox is zoonotic in what animals? What monkeys are particularly susceptible?
• What are the lesions and clinical signs?

Yatapoxvirus

• What are the two yatapoxviruses that affect monkeys?
• What are the typical clinical signs and lesions?
• What species are affected?

Answer 22

Poxviruses

1. Enveloped DNA viruses
2. Monkeypox – Genus Orthopoxvirus
   
   1. OIE reportable
   2. Intracytoplasmic eosinophilic inclusion bodies
   3. Human infections in Africa; US humans secondary to infected prairie dogs that had contact with African rodents
   4. Most important poxviral disease in OWM and NWM
      
      1. OWM at higher risk
   5. Transmission - aerosols, direct contact
   6. CS - maculopapular to nodular lesions on skin → vesiculation and pustules → crust over → fall off → leave scars
   7. Lesions start on extremities and face
   8. Usually respond spontaneously; may be fatal if respiratory involvement (hemorrhagic necrosis)
3. Cowpox virus – Genus Orthopoxvirus
   
   1. Enzootic in rodents - NWM esp callitrichids very susceptible
   2. CS - vesicular hemorrhagic dermal lesions - face, scrotum/labia, palmer/plantar surfaces
   3. Usually fatal
4. Yatapoxvirus –
   
   1. Yaba monkey tumor virus and Yaba-like disease virus – ZOONOTIC
   2. Large eosinophlic intracytoplasmic inclusions (in histiocytes)
   3. YMTV - CS - cutaneous in humans and monkeys, regress after a few months; rhesus monkeys and baboons
   4. YMTV - UNIQUE - Yaba monkey tumor virus - affects histiocytes (not epithelial cells) → SC masses on head and limbs
   5. YMTV - Not seen in NWM

Question 23

Describe the flaviviruses that affect monkeys.

Yellow Fever

• What species are susceptible?
• How is this disease transmitted?
• What are the clinical signs and lesions?

Kyasanur Forest Disease

• What species are susceptible?
• How is it transmitted?
• What are the clinical signs and lesions?

West Nile Virus

• What species are susceptible?
• what are the clinical signs and lesions?

Answer 23

Flaviviruses

1. Yellow fever virus – Genus Flavivirus, Family Flaviviridae
   
   1. Most important viral infection of free-ranging NWM
   2. Mosquitos (Aedes, Haemagogus) - primary vectors
   3. NWM and OWM are reservoirs in sylvatic/jungle cycle - African monkeys subclinical, Asian monkeys + NWM very susceptible
   4. CS - jaundice (hepatocellular necrosis)
2. Monkey fever - Kyasanur forest disease – Genus Flavivirus, Family Flaviviridae
   
   1. Vector - tick borne
   2. Epizootic mortality - black-faced langurs, bonnet macaqeus in India
   3. CS - fever, anorexia, diarrhea

Question 24

Describe the pathophysiology of simian immunodeficiency virus.

What are the natural hosts? How are they affected?

What happens when the virus jumps from a natural host?

How is this virus transmitted?

What is the tropism of this virus?

Is this zoonotic?

Answer 24

Simian immunodeficiency virus (SIV) – Genus Lentivirus

1. Infect CD4+ lymphs and macrophages
2. ZOONOTIC
3. Natural hosts (persistent infection, asymptomatic) - African - chimpanzees, guenons, baboons, mangabeys, vervets, gorillas
4. May progress to SAIDS
5. Asian macaqeus - HIGHLY SUSCEPTIBLE - fatal immunodeficiency
6. Don’t have mixed species exhibits of Asian and African primates
7. Macaque CS - SAIDS - macular rash, lymphadenopath; right atrial and pulmonary thrombosis; enteropathy (villous blunting)
8. Opportunistic infections - cytomegalovirus, Mycobacterium avium-intracellulare, Pneumocystis carinii, Trichomonas, Candida, Plasmodium - due to CD4 T cell loss

Simian immunodeficiency virus (SIV)

Lentivirus

• Epizootiology
  
  • High seroprevalence (76%) in naturally infected primates; higher in adults
  • Strains are genetically diverse
  • Grow in human mononuclear cultures, thus concern about zoonosis
  • Transmission: sexual contact, bite wounds, some vertical transmission
  • New world and prosimians are not natural hosts
• Clinical disease
  
  • Lifelong and clinically inapparent infection
  • Causes disease when jumps from natural host
    
    • Sooty mangabey -> Asian macaque
  • Disease in African species is rare, but can occur with chronic infection
  • SAIDS: simian acquired immunodeficiency syndrome
    
    • Asian primates, especially macaques
    • Meningoencephalitis; lymphoproliferative disease; opportunistic infections as with AIDS (cytomegalovirus, cryptosporidiosis, candida)

Diagnostics

• 3-6 mo for seroconversion
• ELISA: HIV1, HIV 2, SIV specific antigens
• Western blot
• PCR

Human infection

• SIV in chimps origin of HIV1; sooty mangabeys -> HIV2
• 3 human samples positive to SIV, no clinical dz; one seropositive for 11 yrs

Question 25

Describe the pathophysiology of Type D Simian Retroviruses.

What is the tropism of this virus?

What species are highly susceptible? What are the two main serotypes?

How is this disease transmitted?

What are the clinical signs associated with infection?

What are some common secondary infections?

Is this zoonotic?

Answer 25

Simian retroviruses (SRV - historically Type D retroviruses) – Orthoretrovirinae

1. Affects B and T cells
2. Endemic in Asian macaques, langurs; infections in wild, lab, and zoo animals
3. Transmission - horizontal via fighting, sexual contact; vertically; spreads rapidly in a group
4. Immunodeficiency (SAIDS)
5. SRV-1 = rhesus macaques, SRV-2 = pig-tailed and cynomolgus macaques
6. Fatal immunosuppression - persistent diarrhea, weight loss, anemia, pancytopenia; opportunistic infection
7. Common secondary infections - pyogenic bacteria, noma (polymicrobial infection in oral cavity → necrotizing/ulcerative gingivitis/stomatitis with osteonecrosis)
   
   1. Also see CMV, candidiasis, cryptosporidiosis

Type D simian retrovirus (SRV)

Betaretrovirus; it’s an oncovirus too!

• Epizootiology
  
  • High prevalence in wild and captive macaque
  • 5 serotypes: 1-5
    
    • 1,3 (Mason-Pfizer monkey virus): rhesus macaque
    • 2: pigtailed macaque, cynomolgous
    • 4: cynomolgous
    • 5: rhesus from China
  • ‘Endogenous’ in other animals too: squirrel monkey, spectacled langur, yellow baboon. Reported in talapoins (may be endemic)
  • Transmission: not highly transmissible
    
    • Sexual contact, bite wounds, dam-infant

Clinical disease

• SAIDS can develop in chronic infections; macaques usually
• Cutaneous and retroperitoneal fibromatosis
• NOMA=necrotizing stomatitis and osteomyelitis
• Other non-specific signs

Diagnostics

• Culture
• PCR of mononuclear cells

Human infection

• Rare or non-existent in population; 0.48% in macaque workers

Question 26

Describe the pathophysiolgoy of Simian T-Lymphotropic Virus.

What species are commonly affected?

What are the clinical signs and lesions that occur?

Is this zoonotic?

Answer 26

Simian T-lymphotropic viruses or leukemia viruses

1. OWM, asymptomatic typically
2. African green monkeys, baboons - disease reported - lymphoma, leukemia

Simian T-lymphotropic virus (STLV)

Deltaretrovirus

• Epizootiology
  
  • Three groups 1,2 3
  • STLV 1 and 2 close to HTLV 1 and 2
  • Asian and African primates
  • STLV 3 only in African
  • NOT found in New World naturally
  • Transmission: Sexual; vertical possible thru milk
• Clinical disease (STLV-1 only)
  
  • Persistent lymphocytosis, abnormal T cells
  • T-cell lymphomas and leukemia
    
    • Non-Hodgkins lymphoma
  • Skin lesions
  • Splenomegaly

Diagnostics

• ELISA
• Particle agglutination
• IFA
• WB; EIA=Cross reactivity
• PCR

Human infection

• HTLV likely originated from STLV
• HTLV 2 less pathogenic HTLV 1
• STLV positive humans with NHP contact in Africa ONLY
• No seroconversion in NHP workers in US

Question 27

Describe the pathophysiology of Simian Foamy Virus?

What is its host range?

How is it transmitted?

What disease does it cause?

Answer 27

Simian foamy virus (SFV)

Spumavirus

• Epizootiology
  
  • Also isolated from cat, cattle, horse, hamster, sheep, sea lion
  • Widespread with high prevalence (SIV, STLV, SRV are host and range specific)
  • Long history of viral co-evolution
  • Transmission: biting, transfusion, sexual. Vertical likely but not verified (newborns positive but lose status with loss of maternal antibodies).
• Clinical disease
  
  • None
• Diagnostics
  
  • WB
    
    • 2 tests required: monkey antigen and ape antigen
    • Weak cross reaction in both; one alone is insufficient to make diagnosis, thus both together
  • ELISA, IFA, RIPA
  • PCR

Human infection

• Seropositive zoo workers~3%
• No injuries reported with many=casual transmission
• No disease at current report; concern about long latent infections

Question 28

Describe the pathophysiology of gibbon ape leukemia virus & simian sarcoma virus.

What species does each virus infect?

SSV needs what additional virus for replication?

What are the clinical signs associated wtih these viruses?

Is this zoonotic?

Answer 28

Gibbon ape leukemia virus (GaLV)/ Simian sarcoma virus (SSV)

Gammaretrovirus; oncogenic

• Epizootiology
  
  • GALV
    
    • White handed gibbon
    • Transmission: urine/feces, sexual
  • SSV
    
    • N=1 in woolly monkey living with gibbon
    • SSV has defective genome, needs SSAV simian sarcoma associated virus for replication
    • Genetically similar to GALV

Clinical disease

• Lymphoid and myelogenous malignancies
• Osteoproliferative lesions with marrow infiltration
• SSV/SSAV experimentally in marmoset causes fibrosarcomas/fibromas

Diagnostics

• Serology NOT readily available. PCR only.

Human infection

• Serologic evidence with leukemic humans and normal humans; not confirmed with PCR

Question 29

Describe the control of primate zoonoses within a laborotory or zoological setting.

How common is exposure to primate diseases?

Describe a 7 point plan to manage a potential exposure to a simian retrovirus.

Answer 29

EPIDEMIOLOGY

• CDC conducted serosurvey
• SIV, STLV, SRV, SFV tested
• Risk high for persons performing invasive procedures
• Needlestick or mucocutaneous exposure in 35% of workers with avg 7.5 yrs ‘occupational exposure’
• Bigger concern: secondary transmission to human population from infected primate worker

PREVENTION OF ZOONOSES

• Comprehensive occupational health and safety plans
• Safety equipment
• Bite/Wound kits in primate areas (See text for contents)
• *MANAGEMENT OF EXPOSURE**
• The makings of an excellent essay question…*
• Established by team of infectious disease experts (occupational health physician, veterinarian, research personnel, safety officers)
• Standard first aid guidelines; life threatening injury to hospital, bring copy of primate bite protocol
• Immediately clean wound or skin exposure with 15 min gentle scrubbing; eyes or mucous membranes rinse with sterile saline 10 min
• When applicable, apply disinfectant: 0.5% tincture of iodine 10min; rinse with water
• Contact supervisor
• Postcleaning specimen collection with viral culture swab
• Contact health services
• Identify animal
• Let vet know
• Review medical records of animal/group; consider testing strategies for these animals as an institution
• Postexposure prophylaxis for SIV; considered for SRV and STLV

STATUS DETERMINATION OF NHP COLLECTIONS

• Important to know retroviral status of NHP collections
• SIV, SFV, STLV serology
• SRV serology and viral detection in tissues or PCR
• GALV not available
• Consider confirmation by repeat at same lab or compare at different lab
• Screen regularly for seroconversion
• Negative animals can be separated and repeatedly tested to ‘remove’ from cohort or institution
• Prevent contact b/w African and Asian primates
• Not enough information to assess individual risk assessment to determine movement of positive animals to other zoos

Question 30

What is the etiologic agent of callitrichid hepatitis?

What is the reservoir for this virus?

What are the associated clinical signs and lesions?

Is this zoonotic?

Answer 30

Callitrichid hepatitis - lymphocytic choriomeningitis virus - Genus Arenavirus, Family Arenaviridae

1. Acute, fatal epizootic
2. House mouse = reservoir
3. CS - dyspnea, weakness, jaundice
4. Nx - hepatosplenomegaly, pleural/pericard effusion, jaundice, SC/IM hemorrhage
   
   1. ZOONOTIC

Question 31

Describe the picornaviruses that affect monkeys.

Hepatitis A

• What are some commonly affected species?
• How is this disease acquired by NHP?
• What are the associated clinical signs?

Encephalomyocarditis Virus

• What is the natural reservoir of this virus? What other species may carry it?
• What primate species are susceptible? What demographic is most suceptible?
• What are the associated clinical signs and lesions?

Simian Enteroviruses

• What species are commonly affected?
• What are the typical clinical signs and lesions?

Answer 31

Hepatitis A viruses – Genus Hepatovirus, Family Picornaviridae

1. Transmission fecal oral
2. Infection = lifelong immunity, NO chronic hepatitis
   
   1. Serosurvey - infection in marmosets, owl monkeys, cebus, howlers, macaques, African green, chimps

Question 32

Describe the paramyxoviruses that affect monkeys.

Measles

• What species is the natural host?
• How is this disease transmitted?
• What are the clinical signs in OW and NWM?

Parainfluenza Virus

• What species are commonly affected?
• How is this disease transmitted?
• What are the typical clinical signs?

Paramyxovirus Sanguinus

• What species are typically affected?
• How is this disease transmitted?
• What is its origin?
• what are the associated clinical signs?

Answer 32

Measles – Genu Morbillivirus, Family Paramyxoviridae

1. Humans - natural host; can infect OWM and NWM
2. OWM CS - maculopapular exanthema, dry/scaly desquamative dermatitis; ventral body surface, spares plantar/palmar surfaces. May progress to giant cell interstitial pneumonia in OWM
3. NWM - may see epizootics with high morbidity/mortality - no exanthema, necrotizing gastroenteritis primary lesion
4. Immunosuppressive - CMV, bacterial respiratory infection
   
   1. May have false neg intradermal TB skin test after measles infection

Question 33

What is the natural host of simian hemorrhagic fever?

How is it transmitted?

What are the associated clinical signs?

Is ther e a unique lesion?

Answer 33

Simian hemorrhagic fever viruses – Genus Simartevirus, Family Arteriviridae

1. Hosts - African cercopithecines (baboons, patas monkeys, African green monkey)
2. Transmission - social interaction; if African to Asian species → fatal hemorrhagic disease in Asian monkeys
3. Keep Asian and African OWM separates
4. Macaque CS - febrile, facial edema, petechia, SC/retrobulbar hemorrhage, melena, epistaxis
   
   1. Clin Path - consumptive coagulopathy - decreased platelets, abnormal clotting times, elevated LE, hypoalbuminemia
   2. Hematuria, proteinuria

Question 34

Describe the enteric bacteiral pathogens of monkeys.

Shigella

• How is this transmitted? Are there reservoirs?
• What are teh typical clinical signs? How can macaques differ?

Salmonella

• How is this transmitted?
• What are the clinical signs?

Escherichia Coli

• What species are particularly susceptible?
• What are the pathogenic forms of this disease?
• How is it transmitted?
• What are the typical clinical signs?

Yersinia

• What is the reservoir for this bacteria?
• How is it transmitted?
• What species are affected?
• What are the clinical signs?
• Is there a seasonality to this disease?
• What are the lesions?

Answer 34

Shigellosis - Shigella flexneri, dysenteriae, boydii, sonnei - enteroinvasive bacteria

1. Dysentery OWM - large intestine (cecum, colon) - SPARE small intestine
2. ZOONOTIC
3. S. flexneri - also causes ulcerative gingivitis in macaques

Salmonellosis - S. enteritidis, typhinurium

1. Rare in primate colonies; asymptomatic carriers common; clinical cases usually in quarantine
2. CS - moribund, death
3. Necrotizing suppurative enterocolitis
4. ZOONOTIC

Escherichia coli - OWM or NWM

1. Enteropathogenic E. coli - marmoset, tamarins - idiopathic colitis - acute hemorrhagic diarrhea

Yersinia enterocolitica, Y. pseudotuberculosis

1. Reservoir - wild birds, wild rodents
2. Transmission - fecal oral (contaminated feed/water); may become endemic in zoo
3. OWM and NWM, primarily marmosets, tamarins, squirrel monkeys
4. Usually, acute mortality but may be chronic debilitating disease (diarrhea, depression, dehydration)
   
   1. May lead to abortion, stillbirth
5. Seasonal pattern - higher in wet/cold season
6. Nx - GIT, liver, spleen; intralesional colonies of Gram negative bacteria in a necrotic center
   
   1. ZOONOTIC

Question 35

What is the etiologic agent of tularemia?

How is it transmitted?

Answer 35

1. Tularemia - Francisella tularensis
   
   1. Contagious, ZOONOTIC
   2. Transmission - inoculation, ingestion, inhalation; animals housed outdoors at higher risk of exposure
   3. F. tularenisis type A - North America ONLY; type B - throughout northern hemisphere
   4. Lagomorphs (type A) - bite of infected tick or handling/ingesting infected animals
   5. Type B relies on rodents or water contamination - milder form of disease
   6. Seasonal pattern (spring summer)
   7. Typically fatal
   8. CS - depends on form of disease (ulceroglandular (skin, mm, draining LN), pneumonic, typhoidal, septicemic; nx - small granulomas on organs (ddx yersiniosis)

Question 36

Describe the lesions associated with the following respiratory pathogens in monkeys.

Bordetella

• How is this disease transmitted? When does disease occur?
• Which group of primates is more severely affected?
• What are the typical clinical signs?

Klebsiella

• How is this disease transmitted?
• Coinfection with what organism is common?
• What are the typical clincial signs?

Branhamella

• What species is commonly affected?
• What is the unique presentation?
• Is there a seasonality to disease?

Answer 36

1. Bordetellosis - Bordetella bronchiseptica - motile coccobacillus
   
   1. Normal flora of respiratory membranes - attach to ciliary epithelium
   2. Transmission - respiratory; clinical disease - associated w stress
   3. OWM and NWM - more frequent/severe in NWM
   4. Marmosets - mucopurulent nasal discharge, pneumonia - dyspnea, coughing, pyrexia
2. Klebsiella pneumonia - Gram negative aerobe - normal fecal/oral flora
   
   1. May cause invasive abscesses
   2. Transmission - oral or respiratory
   3. Typically concurrent with Pasteurella multocida
   4. Pneumonia, enteritis, septicemia; air sacculitis
3. Branhamella catarrhalis - Blood Nose Syndrome - gram negative - rhesus macaques
   
   1. Epistaxis, periorbital edema, URI; self limiting
   2. Winter, associated with low humidity

Question 37

Discuss the following gram positive infections in monkeys.

Streptococcus pneumoniae

• How is this bacteria transmitted?
• What are the typical clinical signs?

Streptococcus equi zooepidemicus

• How do primates become infected with this organism?

Staphylococcus aureus

• How does infection with this commensal organism typically start?
• What are some of the lesions that can occur?

Answer 37

1. Streptococcus pneumoniae - gram positive coccoid - most common cause of meningitis in NHP
   
   1. Carried in asymptomatic animals/humans in nasopharyngeal mucosa
   2. Transmission - aerosol, fomites
   3. Neuro signs - ataxia, nuchal rigidity, coma
   4. Respiratory - bronchopneumonia followed by arthritis or meningitis (white yellow exudate on brain)
2. Streptococcus equi subsp. zooepidemicus -
   
   1. Primarily young foals, horses - infects NWM/OWM through infected horse meat or keepers as fomites
3. Staphylococcus aureus - commensal of skin, nasopharyngeal mucosa in NHP - gram positive cocci
   
   1. Entry through bite or surgical wound; pustular dermatitis, vaginal infections; sepsis, vegetative valvular endocarditis may lead to emboli
   2. Common beta-lactam resistant

Question 38

Describe the following clostridial diseases in monkeys.

Clostridium tetani

• What is the mechanism of the tetanus neurotoxin?
• How is tetanus transmitted?
• What are the typical clinical signs?

Clostridicum difficile

• What are the clinical signs associated with this infection?
• What are some common predisposing factors for infection?

Clostridium perfringens

• What are the predisposing factors for this infection?
• What are the typical clinical signs?
• What species are particularly susceptible?

Answer 38

1. Clostridium tetani - spore forming obligate anaerobe found in soil - neurotoxin tetanospasmin - blocks release of GABA at neuromuscular junction → muscle spasms
   
   1. Transmission - contaminated wounds
   2. CS - torpor, reluctance to interact, bipedal locomotion, hopping/falling, piloerection, progressive stiffness; advanced - trismus, opisthotonus, seizures; fatal secondary to resp paralysis
2. Clostridium difficile - normal flora - overgrowth → cytotoxin production → pseudomembranous colitis
   
   1. Antibiotic associated diarrhea - prolonged beta-lactam use or stress/chronic disease
3. Clostridium perfringens - acute gastric dilatation / bloat syndrome
   
   1. Occurs after overeating and drinking, after anesthesia, after abx disrupt gut flora
   2. CS - abdominal distention secondary to gastric dilation, SI full of gas/fluid; acute shock syndrome, could die secondary to dec venous return
   3. OWM (cercopithecine, colobine), NWM

Question 39

List four of the mycobacteria species that affect monkeys.

What is the etiologic agent of tuberculosis?

• How is it transmitted?
• Which monkeys have more severe disease? Are any subclinical carriers?
• What are the typical clinical signs?

What effects does infection with Mycobacterium kansaii have clinically?

Immunosuppressed monkeys are susceptible to what additional mycobacterial infections?

What is the etiologic agent of Johne’s?

• What monkey species are susceptible to infection?
• What are the typical clinical signs?

What is the etiologic agent of Leprosy?

• What are the lesions?
• How is it transmitted?

Answer 39

1. Mycobacterium tuberculosis, M. bovis - intracellular Gram variable, acid fast
   
   1. ZOONOTIC, anthropozoonotic
   2. Transmission - aerosol, ingestion; once in a colony, spreads rapidly with high morbidity/mortality (epizootic event)
   3. Most severe outbreaks usually in OWM
   4. Cynomolgus monkeys - subclinical disease
   5. CS - coughing, weight loss
2. Mycobacterium kansaii - atypical environmental - not usually associated with clinical disease
   
   1. False positive on intradermal TB test
   2. Transmission - inhalation
   3. May have abscessation of pulmonary LN
3. M. avium complex - M. avium and M. intracellulare - environmental - severe infection in immunosuppressed animals
4. M. avium subsp. paratuberculosis - progressive diarrhea and weight loss
   
   1. Transmission - water, soil, paratenic insects
   2. Positive TB test may occur
   3. OWM more susceptible than NWM
   4. Frequently seen in SAIDS
   5. Thickened colon/small intestine, ileocecocolic jxn - represent Johne’s in cattle - intrahistiocytic acid fast positive bacilli
   6. Respiratory tract rarely site of infection
5. M. leprae - leprosy - chronic granulomatous disease - skin and peripheral nerves affected - histiocytic, intralesional acid fast bacilli
   
   1. Transmission - respiratory, infected skin lesions
   2. Nodular thickening of skin and peripheral nerves → paralysis/deformities face, hands, feet on cooler areas of body (ears, nose, scrotum, tail)

Question 40

Describe the common fungal diseases of monkeys.

What is the most commonly diagnosed fungal infection?

Pneumocystis

• What species are commonly affected?
• How are these organisms confirmed cytologically or histologically?
• What are the common clinical signs?

Systemic Fungal Infections

• What species are commonly affected by Coccidiodes and Histoplasma?
• What species are commonly affected by Cryptococcus?
• What are the geographic locations of the common systemic fungal infections?

Owl Monkey Fungus

• What is unique about owl monkey fungus?
• What are the typical clinical signs?

Microsporidiosis

• What microsporidia can infect monkeys?
• How are these transmitted?
• What are the clinical signs of affected animals?

Answer 40

Fungi

1. Most commonly diagnosed - candidiasis
2. Pneumocystis jirovecii or carinii - opportunistic - silver stain
3. Systemic - Cryptococcus neoformans, Coccidiodes immitis, Histoplasma capsulatum var capsulatum, Paracoccidioides brasiliensis
4. Dermal - Sporothrix schenkii, Histoplasma capsulatum var duboisii

Question 41

Describe the following nematode parasites of monkeys.

Strongyloidiais

• What parasite species are these?
• What monkey species are commonly affected?
• What is teh general life cycle?
• What are teh typical clinical signs?

Oxyuriasis

• What are the pinworms of OW monkeys? What about NW monkeys?
• What is the general lifecycle and pathology?

Oesophagostomiasis

• What is the general life cycle and pathology?

What species and what lesions typically occur with infection with Ternidens diminutus?

What group of primates are affected and what lesions occur with Ancylostoma or Necator infestation?

What parasite causes hemorrhagic or ulcerative enteritis adn pancreatitis? What species are affected?

What two nematodes can be transmitted by cockroach ingestion? What are the clinical signs they cause?

Physlopteriasis affects which species and causes what lesions?

Answer 41

Question 42

Describe the nematodes & trematodes that affect monkeys.

Filiariasis

• What filariad nematodes affect monkeys?
• What monkey species are commonly affected?
• How are they transmitted? What is the general life cycle?
• What are the lesions and clinical signs they cause?

Anatrichosomiasis

• What monkey species are affected by anatrichosoma?
• What is the general life cycle?
• What are the lesions and clinical signs?

Acanthocephalans

• What acanthocephalans affect monkeys?
• What species are commonly affected?
• How are they trasmitted? What is teh general life cycle?
• What are the lesions and clinical signs?

Schistosomiasis

• What monkey species are commonly affected?
• What is the general life cycle? How are they infected?
• What are teh lesions and clinical signs?

Dinobdelliasis

• What monkey species are commonly affected?
• Whats the general life cycle?
• What are teh clinical signs and lesions?

Answer 42

Question 43

Discuss the cestodes that affect monkeys.

Hydatidosis is caused by which cestodes?

• What is the definitive host?
• What can occur if the cysts rupture?

Cysticercosis is caused by which cestode?

• What is the definitive host?
• Symptoms are secondary to what?

Answer 43

Metazoan Parasites

1. Hydatidosis - echinococcosis - larval cestodes - Echinococcus sp.
   
   1. Definitive host - canids
   2. E. granulosus - Cysts form and produce brood capsules within that hold protoscolices and calcareous corpusculesProtoscolices - acid fast hookles, 4 suckers; when cysts rupture, seed body cavities
   3. E. multilocularis - OWM - fox tapeworm
      
      1. Definitive host - red fox; intermediate host - rodents
      2. Forms multiple small budding cysts (look like alveoli)
      3. Protoscolices implant on other tissues when cysts rupture
      4. Ruptured cysts - anaphylactic reaction
2. Cysticercosis - Taeniidae cestodes
   
   1. Cysticerci - cysts that contain single invaginated larval scolex with 4 suckers in peritoneal or pleural cavity
   2. Symptoms secondary to space occupying cyst
      
      1. Definitive host - canids

Question 44

Describe the protozoa that affect monkeys.

Toxoplasmosis

• What groups of primates are more susceptible?
• What are teh typical clinical signs and lesions?

What are the clinical signs of Trypanosomiasis in Monkeys? Where are animals typically affected (geographically)?

What is the etiologic agent of amoebiasis in monkeys?

• Which group is more affected?
• What clinical signs and lesions occur? How does this differ by species?

What is the etiologic of amoebic encephalitis?

What is the etiologic agent of malaria in monkeys?

Answer 44

Protozoan Parasites

1. Toxoplasmosis - highly virulent NWM
2. Epizootic - squirrel monkey
3. Transmission - feed contaminated with infective feline oocysts; consumption of infected rodents; consumption of paratenic hosts (meat, insects, earthworms)
4. Wild primates rarely seropositive
5. Nx - pulmonary congestion, pulmonary edema, splenomegaly, mesenteric lymphadenitis
   
   1. Tachyzoites - necrotic lesions
   2. Bradyzoites - tissue cysts in chronic lesions

Question 45

Describe the arthropod parasites that infest monkeys.

What is the etiologic agent of pulmonary acariasis?

• How is it transmitted?
• What clinical signs may occur?
• Where is it commonly found?
• How is it treated?

What is the etiologic agent of nasal acariasis?

• What lesions do they cause?

What are three ectoparasitic mites?

Answer 45

Arthropod Parasites

1. Pulmonary acariasis - lung mites - feed on pulmonary epithelial cells, erythrocytes, lymph
2. Pneumonyssus simicola - most common - OWM
3. 100% prevalence in wild-caught; low incidence in born/raised in managed care
4. Transmission - inhalation, ingestion via grooming, feces
5. No CS; predispose to bacterial infection (imapired mucociliary clearance)
6. Predilection for cranial lobes
7. Administer prophylactic ivermectin
8. Nx - multifocal gray-yellow thin cysts
   
   1. Intralesional golden brown birefringent granular pigment in peribronchiolar and peribronchial inflammation = mite excrement (large granules of hemosiderin, lipofuscin)

Question 46

A recent study evaluated vitamin D levels in seven platyrrhine species housed in a UK zoo.

What group of primates is more susceptible to calcium metabolism disorders?

What are the possible mechanisms for that increased need?

Did the summer and winter values of vitamin D3 differ?

Answer 46

Killick, R., Saunders, R., & Redrobe, S. P. (2017). Summer and winter vitamin d3 levels in seven platyrrhine species housed at a british zoo, with reference to natural uvb levels. Journal of Zoo and Wildlife Medicine, 48(3), 732-741.

Abstract: Serum samples were collected from 24 platyrrhines of seven diurnal species housed with outdoor access at Bristol Zoo Gardens (United Kingdom) to test 25-hydroxyvitamin D3 (25OHD3) levels as part of the veterinary department’s preventative health care program. Samples were collected in August 2008 (summer) and January 2009 (winter) to examine the effect of season on 25OHD3 levels. Dietary levels of vitamin D3 remained the same throughout the study period and fell within the range of 2000–4000 IU/kg dry matter, in accordance with current primate guidelines. Statistical analysis showed that there was no significant difference between the platyrrhines’ summer 25OHD3 values (range < 4.0–> 50.0 ug/L) and winter 25OHD3 values (range <4.0–80.1 ug/L). However, ultraviolet B (UVB) measurements taken at the zoo during the study period confirmed that UVB levels were significantly higher in summer (mean reading for 1200–1300 hours GMT time period, 153.8 lW/cm2) compared with winter (mean reading for 1200–1300 hours GMT time period, 19.4 lW/cm2). The 25OHD3 levels measured were generally found to be low compared with previously published values from healthy captive and wild platyrrhines.

• NW primates more susceptible to calcium metabolism disorders – relative resistance to active D3 (1,25 di-OH)
• Platyrrhines can exhibit Vitamin D levels that would be consistent with hypervitaminosis D in OWP
• Platyrrhines overexpress vitamin D binding protein – possibly from plant with a 1,25OHD glycoside in SA or from high UVB exposure – latter make sense as nocturnal owl monkeys don’t have such high levels
• Husbandry needs – high Vitamin D (300 IU/kg DM – still produced disease) and natural UVB exposure needed
• Saki, Geoffroy’s marmoset, & GLT had higher D3 in the summer; squirrel monkeys, Goeldi’s monkeys, GHLT, & BLT did not
• D3 levels were low in all seasons

Take Home:

• Natural UV light should not be depended on to boost D3 levels in platyrrhines – the diet needs to provide it

Question 47

A recent paper describe strategies to manage psychopathologies in primates in managed care.

What are some of the adverse behaviors monkeys may show?

What are some of the possible factors of developing psychopathologies?

What are five general treatment strategies?

Answer 47

Kummrow, M. S., & Brüne, M. (2018). Psychopathologies in captive nonhuman primates and approaches to diagnosis and treatment. Journal of Zoo and Wildlife Medicine, 49(2), 259-271.

Abstract: Despite the growing knowledge and literature on primate medicine, assessment and treatment of behavioral abnormalities in nonhuman primates (NHPs) is an underdeveloped field. There is ample evidence for similarity between humans and great apes, including basic neurologic physiology and emotional processes, and no substantial argument exists against a concept of continuity for abnormal conditions in NHPs that emerge in response to adverse experiences, akin to human psychopathology. NHPs have served as models for human psychopathologies for many decades, but the acquired knowledge has only hesitantly been applied to primates themselves. This review aims to raise awareness among the veterinary community of the wealth of literature on NHP psychopathologies in human medicine and anthropology literature and calls for the necessity to include mental health assessments and professionally structured treatment approaches in NHP medicine. Growing understanding about causes and pathogenesis of abnormal behavior in NHP will not only help to prevent the development of undesirable behaviors but also allow for treatment and management of long-lived, already affected animal patients.

• Normal vs not normal.
  
  • Impossible to apply behavioral assessments for wild NHP to captive NHP.
  • Behavior related to environmental circumstances, would differ in captivity vs wild conspecifics.
• Pragmatic approach for comparing human with NHP conditions use criteria of cross-cultural approaches:
  
  • Persistence and exclusion of any given context.
  • Disruption of flow in an individual’s life.
  • Psychological or somatic distress or both.
  • Significant behavioral alteration relative to an understood social and cultural space indicative of a pathologic condition.
• Motor stereotypic behaviors – pacing, circling, flipping, head tossing. Repetitive behavior induced by frustration, repeated attempts to cope and/or brain dysfunction. Amount of time of social deprivation, husbandry, space limitations, and lack of environmental control are causal factors.
  
  • However, reduction of a stereotyped behavior may mean prevention of a coping mechanism and be detrimental to the individual if underlying triggers are not eliminated.
• Self-injurious behavior – plucking hair, skin picking and scratching, head banging, self-biting. Coping strategy to reduce arousal and distress.
  
  • Reinforcement by neuroendocrine changes.
  • Early life trauma assoc with increased vulnerability to SIB in both nonverbal humans and NHPs.
• Regurgitation and reingestion – expulsion of food in absence of nausea and abdominal muscular contractions.
  
  • Possibly associated with social behavior. Increased meal frequency or provision of consistently available edible material may be effective in the reduction of R&R.
• Coprophagy – deliberately eating feces.
  
  • Balance between benefits of coprophagy i.e. provision of vitamins and intestinal symbionts and detrimental effects i.e. transmission of parasites still required.

Etiology and pathogenesis of psychopathologies:

• Hereditary basis for wide range of psychiatric disorders in humans.
• Male sex and young age ID as intrinsic risk factors to develop MSB in NHP.
• Stress triggers acute sympathetic-adrenomedullary system, results in release of NE and cortisol.
  
  • beta-endorphin released with ACTH.
• Decreased serotonin associated with affective illnesses and depression in humans and animal models.
• Extrinsic risk factors may be grouped:
  
  • Adverse childhood events i.e. early maternal separation.
    
    • Self-injurious behaviors common following early maternal separation.
  • Suboptimal conditions in captivity and external stressors.
  • Acquired dysfunction of brain structures.
• Lack of control may trigger MSB or SIB or learned helplessness – lethargy, anorexia, inhibition of exploratory behavior, aberrant immune responses.
  
  • Management modifications allowing for individual control of environmental or social factors crucial for welfare.
  • Predictability of events also important.
• Pathologic neurodegenerative, age-related processes i.e. Alzheimer in humans.
  
  • Amyloid deposits associated with difficulties in object recognition, visuospatial orientation, delayed reaction time in animals.
  • Inflammatory processes of CNS, auto-immune dz may contribute.
  • Pathologic behavior may be culturally transmitted between group members, constitute learned behaviors.

Diagnosis of psychopathologies:

• Behavioral observations.
• Standardized documentation.
• Frequency and intensity of target behaviors.
• Noninvasive fecal glucocorticoid hormone sampling.

Treatment options for psychopathologies:

• Five broad forms of approaches to abnormal behavior in captive animals:
  
  • Genetic selection.
  • Behavioral therapy.
    
    • Positive reinforcement training.
  • Physical prevention.
    
    • Not only reducing abnormal behavior but also simultaneously shaping more desirable behaviors as alternative coping mechanisms. Counterconditioning.
  • Environmental enrichment.
    
    • Food-based, occupational, structural, sensory, social.
      
      • Match level of cognitive challenge to the animal’s skills.
      • Produce satisfaction without anxiety, apathy, or boredom.
  • Pharmacologic treatment.
    
    • Target opiate, serotonergic, and dopaminergic systems.
      
      • Serotonin can be regulated at three levels – synthesis, reuptake, postsynaptic.
        
        • Availability of amino acid tryptophan and modulation of tryptophan hydroxylase activity directly influence synthesis in the serotonergic neuron.
          
          • Inhibition by SSRIs i.e. sertraline, fluoxetine, citalopram or dual serotonin-norepi uptake inhibitors like SNRIs and MAO-A inhibitors increase extracellular serotonin levels.
          • Serotonin receptor agonists and antagonists increase or decreases effects at the postsynaptic neuron, respectively.
          • Supplementation of tryptophan may increase availability of the precursor.
    • Chlorpromazine blocks dopamine receptors. Also haloperidol.
    • Naltrexone modulates endogenous opioid system.
    • Benzodiazepines used to control acute episodes of abnormal behavior.
    • Results of these meds are inconsistent/spp dependent.
    • Gabapentin
    • Cyproterone acetate CA reduced levels of SIB in male rhesus macaques.
      
      • Mechanism unknown, possibly due to progestin activity of CA decreasing testosterone or inhibition of MAO-A.
      • Alpha 2 receptor agonists have been used in humans.
        
        • Also in rhesus macaques (guanfacine) to control self-biting, dose dependent, mechanism not completely understood.
    • Combination therapies not routinely used in primates, common in humans.
  • Combined therapy of adjusted environment, inanimate as animate, behavioral therapy, and adapted interactions with human caregivers and supporting pharmaceutic therapy may serve as an individually tailored approach to increase welfare.
  • Genetic selection for better coping with challenging situations may have to be increasingly considered for breeding decisions in zoos.

Question 48

A recent paper described diffuse idiopathic skeletal hyperostosis in a spider monkey.

What is DISH?

How did this animal present?

Answer 48

Ratliff, C., Waller, K. R., Steinberg, H., & Clyde, V. L. (2020). DIFFUSE IDIOPATHIC SKELETAL HYPEROSTOSIS WITH SECONDARY DYSPHAGIA IN A BLACK-HANDED SPIDER MONKEY (ATELES GEOFFROYI). Journal of Zoo and Wildlife Medicine, 51(2), 455-458.

Abstract: A 32-yr-old male black-handed spider monkey (Ateles geoffroyi) with marked kyphosis and reduced spinal range of motion developed intermittent regurgitation, which was managed with an acid reducer. Diffuse idiopathic skeletal hyperostosis (DISH) was suspected in this animal due to radiographically evident ossification of the anterior longitudinal ligament. At repeat radiographic evaluation 1.5 yr later, due to weight loss and increased frequency of regurgitation, the cervical spine was deviated ventrally and appeared to be impinging on the thoracic inlet. The spider monkey was humanely euthanized due to poor prognosis, and the presumptive diagnosis of DISH was confirmed via postmortem computed tomography and necropsy. DISH has not been reported in black-handed spider monkeys, and secondary dysphagia, an uncommon but recognized consequence in humans, has not been reported in a nonhuman primate. Earlier recognition of this possibly underreported disease process may increase treatment options and effectiveness of intervention.

• Geriatric black-handed spider monkey, marked kyphosis of spine first documented at 13yo.
• Immobilized for workup of regurgitation and vomiting.
• Rads – Progressive ankylosing spondylosis with bridging of entire thoracolumbar spinal column and thickening of ossified anterior longitudinal ligaments.
• Upper GI endoscopy – Highly motile esophagus, cardia of stomach tight and difficult to enter.
• Vit D testing lower vs others tested, PTH measured elevated vs others.
  
  • Consistent with mobilization of bone.
• Intermittent regurg managed with famotidine for about 1.5 yrs. Euthanized.
• CS – Generalized loss of fine trabeculation and diffuse thickening of cortices, consistent with disuse osteoporosis and osteopenia. Marked amount of smooth chronic ankylosing bone formation along anterior longitudinal ligament completely bridged spinal column from T3-L7, preserving intervertebral disk spaces and not affecting articular facets, leading to a diagnosis of diffuse idiopathic skeletal hyperostosis over other causes of spondylosis.
  
  • Lack of typical sacroiliac involvement and preservation of joint spaces made ankylosing spondylitis unlikely in this case.
  • Sequelae – Pain, decreased mobility, dysphagia, airway obstruction, or aspiration pneumonia.
  • Mass effect from hyperostosis of anterior longitudinal ligament or severe kyphosis resulting in mechanical obstruction of esophagus.
• DISH – Syndrome whereby multifocal ossification of fibrous soft tissues occurs, typically in spine and associated ligaments and joint capsules. Advanced age risk factor in humans.
  
  • Often asymptomatic, progresses to stiffness and decreased range of motion as extensive portions of the spine effectively fuse together.
  • No known reports of DISH in other zoologic species, rare in dogs and cats.

Question 49

A recent study described surgical management of endometriosis in macaques.

What is endometriosis?

What species are commonly affected? How do these cases typically present?

What are the two treatment options?

What surgical technique did this paper describe? How successful was it?

Which macaques did the best with the procedure?

Answer 49

Kennedy, L. H., Nowland, M. H., & Nemzek-Hamlin, J. A. (2019). Surgical treatment of spontaneous endometriosis in rhesus macaques (Macaca mulatta): 11 cases (2007–2011). Journal of the American Veterinary Medical Association, 254(12), 1454-1458.

OBJECTIVE To determine long-term outcome for rhesus macaques (Macaca mulatta) with endometriosis that underwent surgical treatment and identify factors potentially associated with long-term outcome.

DESIGN Retrospective case series.

ANIMALS 11 female rhesus macaques.

PROCEDURES Medical records of female rhesus macaques in which endometriosis was diagnosed between 2007 and 2011 and that underwent abdominal exploratory surgery were reviewed.

RESULTS In 5 macaques, the only clinical abnormality was a caudal abdominal mass identified during a routine physical examination, and in 6 macaques, overt clinical signs of endometriosis, including anorexia, dysmenorrhea, and lethargy during menses, were reported. Five macaques had histologically confirmed complete ovarian removal, and another 5 had incomplete ovarian removal (ovarian tissue was not examined histologically in 1 macaque). Nine animals survived at least 12 months after surgery, and 6 survived at least 60 months after surgery. Macaques that did not have overt clinical signs were significantly more likely to survive at least 60 months after surgery. However, extent of ovarian removal was not significantly associated with survival 12 or 60 months after surgery.

CONCLUSIONS AND CLINICAL RELEVANCE Results suggested that, in select situations, surgery (ovariectomy or ovariohysterectomy) may be curative in macaques with endometriosis and may result in long-term survival. Further, findings suggested that monitoring until clinical signs appear before performing surgery is not warranted in adult female macaques suspected to have endometriosis that only have a caudal abdominal mass and no other overt clinical signs.

Spontaneous endometriosis

• Reported in multiple nonhuman primate species
• Most commonly - macaques and baboons
  
  • Prevalence rates as high as 30% reported in female macaques
• Characterized by ectopic endometrial tissue outside of uterus that advances and regresses under hormonal influence
• Macaques - most commonly leads to dysmenorrhea and anorexia, may cause abdominal pain secondary to adhesions
• Reported to cause death in nonhuman primates
• Major risk factor for spontaneous hemoperitoneum in pregnancy
• Treatment
  
  • Ovariectomy - considered curative in macaques because estrogen required for ectopic tissue to proliferate
    
    • Success rate following surgery reported to be low as 60% in macaques
    • Success rate possibly correlated with severity of disease at surgery
    • High risk of ovarian remnants due to adhesions and difficulties associated with identifying ovaries
  • Medical management - alternative to surgery in NHP
    
    • Many hormonal treatments can have undesirable effects or difficult to administer properly
    • Medroxyprogesterone acetate – standard treatment
    • Alters glucoregulatory function in macaques

Objective - determine long-term outcome for rhesus macaques with endometriosis following surgical treatment and identify factors potentially associated with long-term outcome

• 11 rhesus macaques underwent ovariectomy or ovariohysterectomy for treatment of endometriosis
• In select situations, ovariectomy or ovariohysterectomy may be curative in macaques with endometriosis and may result in long-term survival
• Macaques where endometriosis was incidental were significantly more likely to survive at least 60 months after surgery, compared with macaques that had overt clinical signs
  
  • All 5 macaques euthanized ≤ 18 months after surgery had overt clinical signs of endometriosis
• Increasing age - risk factor for endometriosis
  
  • All animals with endometriosis were older (15-24 years)
  • 9 of 11 survived at least 12 months after surgery
  • 6 of 11 survived at least 60 months after surgery
  • Even with complete ovarian removal, lesions already present unlikely to regress, and severe lesions can cause further complications

Question 50

A recent study investigated the prevalence of entamoeba in macaques in Taiwan in areas with high human traffic.

What are the clinical signs associted with Entamoeba histolytica infection?

Was there any risk of transmision to humans?

Answer 50

Chang, A. M., Chen, C. C., & Huffman, M. A. (2019). Entamoeba spp. in wild formosan rock macaques (macaca cyclopis) in an area with frequent human-macaque contact. Journal of wildlife diseases, 55(3), 608-618.

ABSTRACT: Entamoeba is a genus of gastrointestinal protozoon that is transmitted through contaminated food and water. This protozoon is commonly found in human and nonhuman primates. Contact between humans and Formosan rock macaques (Macaca cyclopis) has become more frequent due to food provisioning; accordingly, concerns regarding zoonotic pathogen transmission through the fecal-oral route have increased. For example, surveillance of intestinal parasites in wild Formosan rock macaques indicated that Entamoeba infection was the most prevalent type of intestinal parasite infection. The morphologies of pathogenic and nonpathogenic species are difficult to distinguish. In this study, we collected fecal samplesfrom wild Formosan rock macaques in the Shoushan National Nature Park (Kaohsiung, Taiwan) and adopted both morphologic and molecular methods for Entamoeba species identification. In total, we collected 208 fecal samples with a 57.7% (120/208, 95% confidence interval: 50.9–60.4%) prevalence of Entamoeba infection. Four Entamoeba species were identified: three nonpathogenic species, Entamoeba coli (19%), Entamoeba chattoni (50%), and Entamoeba hartmanni (11%), and one potentially pathogenic species, Entamoeba nuttalli (20%). Our study revealed the risk of zoonotic transmission of these Entamoeba species to humans. To address relevant public health and wildlife conservation concerns, further research is required to fully understand the virulence of E. nuttalli isolated from Formosan rock macaques.

• E. histiolytica causes hemorrhagic dysentery, liver ulcers, extra-intestinal lesions, death
• Amoebiasis second leading cause of death by parasites in humans
• Morphologically E. histolytica, E. nuttalli, E. dispar are indistinguishable

STUDY DESIGN: Fecal samples collected from unidentified individuals over 1 year in the national park. Performed sedimentation technique for microscopic ID and evaluated molecular PCR

• Sequenced and banked for the four identified Enamoeba species
• Created phylogenetic trees compared to sequences from GeneBank
• Human isolations were mixed with NHP isolations in various subclades—indicate possibility of transmission
• High prevalence of Entamoeba infection in NHPs; most common protozoal infection in NHPs
• Drinking water may be contaminated

Question 51

A recent study described the reproductive lesions of female japanese macaques.

What was the most common lesion identified?

What was the most common uterine neoplasm identified?

What is endometriosis? How does it occur?

What are the clinical signs?

How is it managed?

Answer 51

Gall, A. J., Olds, J. E., Wünschmann, A., Selmic, L. E., Rasmussen, J., & Lewis, A. D. (2018). LESIONS OF THE FEMALE REPRODUCTIVE TRACT IN JAPANESE MACAQUE (MACACA FUSCATA) OF TWO CAPTIVE COLONIES. JZWM 49(1), 79.

Abstract: Reproductive lesions have been described in various nonhuman primate species, including rhesus macaques (Macaca mulatta), cynomolgus macaques (Macaca fascicularis), baboons (Papio spp.), squirrel monkeys (Saimiri sciureus), and chimpanzees (Pan spp.); however, there are few publications describing reproductive disease and pathology in Japanese macaques (Macaca fuscata). A retrospective evaluation of postmortem reports for two captive M. fuscatapopulations housed within zoos from 1982 through 2015 was completed, comparing reproductive diseases diagnosed by gross pathology and histopathology. Disease prevalence, organs affected, and median age at death between the two institutions was also compared. Fifteen female captive M. fuscata, ranging in age from 15 to 29 yr were identified with reproductive tract lesions, including endometriosis, endometritis, leiomyoma, leiomyosarcoma, and adenomyosis. No significant differences were identified in disease prevalence, organs affected, and median age of death between the two institutions. Endometriosis was the most common disease process identified and was found in 10 of the 15 cases (66.7%), followed by leiomyoma (4 of 15; 26.7%). In four cases (26.7%), severe endometriosis and secondary hemorrhage was indicated as the cause of death or the primary reason for humane euthanasia. These findings were compared with a separate population of Japanese macaques managed within a research facility in the United States, with a prevalence of endometriosis of 7.6%. This study discusses possible risk factors and potential treatment options for the management of endometriosis in captive M. fuscata.

• Female Japanese macaques est life span 25 yrs.
• Reproductively mature 2-4 yrs age.
• Most fecundity between 5-19 years, although parturition documented up to 25yo.
  
  • Retrospective – necropsy reports, two zoological institutions.
    
    • Adult, female JM died between 15-30 yrs. 15 cases.
    • 14 had reproductive tract lesions, with 8 having multiple areas affected.
    • 86% lesions in uterus. Grossly characterized as either individual, firm, beige, delineated, or infiltrative masses in uterine wall or firm, beige, poorly defined, and frequently confluent nodules of the uterine wall and adjacent mesometrial adipose.
    • Endometriosis in 10 individuals, assoc with hemorrhage in some. One assoc with uterine rupture. Hemoabdomen, hemothorax in one. Intrapelvic masses assoc with endometriosis caused compression of colon, displacement of bladder.
    • 6 neoplastic conditions – uterine leyomyomas, leyomyosarcoma, ovarian granulosa cell tumors.
    • Extent of lesions did not correlate with numbers of offspring.
    • No differences in age at death between the two institutions.
  • Discussion:
    
    • Endometriosis – Chronic, hormonally responsive endometrial glands and stroma located ectopically outside the uterus, most commonly in the pelvic peritoneum, ovaries, rectovaginal septum.
      
      • Sampson Hypothesis – Theory that endometriosis arises from retrograde menstration through fallopian tubes into the peritoneal cavty.
      • CS – decreased fertility, ectopic tissue formation, abdominal discomfort, defective ovarian function, menstrual irregularity, embryo implantation failure, excessive uncontrollable hemorrhagic conditions.
      • Most commonly recognize gynecologic dz of menstruating NHP.
      • In humans – associated with advanced age, parity, past surgical interventions, long periods of time of uninterrupted menstrual cycles, exposure to toxins and radiation, and genetic predisposition.
      • Based on these institutions – long periods of uninterrupted cycling and genetic variables.
      • Hemorrhage may result in hypovolemia, circulatory collapse, cardiac arrest, hepatic necrosis.
      • Possible treatments – Surgical management can be conservative i.e. preservation of fertility or resecting all ectopic tissues, adhesions, reconstruction of pelvic anatomy. Or can be definitive – complete hysterectomy or bilateral oophorectomy with resection of all ectopic endometrial tissues, prevents reocurrence.
        
        • Conservative more common to preserve fertility.
        • Medical – Hormonal alteration i.e. GnRH agonists, progestin-based treatments. May be assoc with vasomotor symptoms, bone mineral density changes, CV risks.
    • This study contrasts with another research institution, most common diagnoses were endometriosis and uterine leiomyoma.
    • Most common neoplasia in female NHP – uterine leiomyomas.
      
      • Benign, arise from smooth muscle within uterine wall.
      • Second most common is endometrial adenocarcinoma.

Question 52

A recent report described impetigo in red-tailed monkeys.

What is impetigo? What pathogens typically cause it?

What are the typical clinical signs and lesions?

What are some predisposing factors to acquiring impetigo?

Answer 52

Coughlin, P., Bradford, C., Montali, R. J., & Bronson, E. (2018). Pustular dermatitis caused by impetigo in red-tailed monkeys (cercopithecus ascanius). Journal of Zoo and Wildlife Medicine, 49(1), 206-209.

Abstract: Impetigo is a bacterial infection of the superficial layer of the epidermis with crusting or bullae caused by Streptococcus spp., Staphylococcus spp., or both. A 14-yr-old red-tailed monkey (Cercopithecus ascanius) presented with recurrent scabbing and ulceration under the nares over an 8-yr period. Repeated cultures and biopsy samples led to a presumptive diagnosis of impetigo, later confirmed on necropsy. Multiple antibiotic regimens were employed with varying success during multiple episodes, while lesions resolved on their own at other times. This condition has not been previously reported in a nonhuman primate, although it is not uncommon in humans.

Brief Communication

• 14yo vasectomized male red-tailed monkey, bilateral scabbing philtrum intermittent, progressed to ulcerations and mild hemorrhage when in separate holding area. Bx consistent with pustular cheilitis with large numbers of G+ cocci. IHC for herpes negative.
• Another biopsy performed over a year later due to continued clinical signs.
  
  • Some improvement with ciprofloxacin. Female conspecific started having similar clinical signs. Bx showed perivascular dermatitis, epidermal necrosis and vasculitis, Staph spp.
  • Presumptive dx of impetigo was made.
• Impetigo
  
  • Staphylococcal-associated pustular dermatitis, recurs over extended time period.
  • Hallmarks – nonpainful, generally nonpruritic, superficial pustules, do not involve fair follicles, appear in sparsely haired areas of skin.
    
    • Histo – Neutrophilic subcorneal pustules with intralesional cocci without acantholytic keratinocytes in the epidermis.
      
      • Typically caused by coagulase-positive staph i.e. S. intermedius, Sp. pyogenes may also be implicated.
      • May be redisposed to recurrent infections.
    • Happens in immunocompromised humans i.e. children. May be associated with periods of increased stress.

Ddx – immune-mediated conditions i.e. pemphigus-foliaceous, herpesviral infections, allergic or contact dermatitis. Other common skin issues in NHP – Dermatomycoses, ectoparasites i.e. Demodex, Sarcoptes, trauma from conspecifics, herpesvirus-related lesions (vesicle and ulcer formation), and cutaneous manifestations of endocrinopathies i.e. hypothyroidism and diabetes mellitus.

Question 53

A recent report described cutaenous demodicosis and UV-induced skin neoplasia in two Goeldi’s monkeys.

Why do these monkeys need higher levels of UV exposure?

How did the skin gradually progress towards cancer?

What is the maximum intensity of UV light needed to prevent rickets?

What predispoed these areas to demodicosis?

Answer 53

Gruber-Dujardin, E., Ludwig, C., Bleyer, M., Kaup, F. J., & Mätz-Rensing, K. (2019). Cutaneous demodicosis and uv-induced skin neoplasia in two goeldi’s monkeys (callimico goeldii). Journal of Zoo and Wildlife Medicine, 50(2), 470-473.

Abstract: Two nonrelated Goeldi’s monkeys (Callimico goeldii) from the same enclosure developed multifocal alopecia with hyperkeratotic to ulcerative skin lesions on the lower abdomen and inner thighs. Necropsy samples of the first animal showed hyperplastic dermatitis together with in situ carcinoma and intralesional Demodex organisms. The second monkey developed similar lesions 2.5 yr later. Skin scrapings and biopsies also revealed Demodex mites within hyperplastic dermatitis. Long-term treatment with ivermectin, imidacloprid-moxidectin, and sarolaner resolved the demodicosis but skin lesions progressed to actinic keratosis and carcinoma. Both cutaneous neoplasia and demodicosis are rarely described in New World monkeys and these are the first reported cases in Goeldi’s monkeys. Since the animals had access to ultraviolet (UV) light, as recommended for indoor-housed callitrichids, the skin tumors were likely UV-induced and the mites have settled particularly within impaired regions. Thus, apparent demodicosis can indicate cutaneous immunosuppression and might alert caretakers to adjust the UV regime.

• Gradual progression from epithelial hyperplasia to precancerous actinic keratosis to in situ carcinoma to SCC is strongly suggestive of cumulative exposure of UV radiation as the underlying cause.
• Maximum intensities of 80-120 microW/cm^2 at distance of 100 cm regarded as sufficient for rickets prevention.
• UV-induced immunosuppression by impairment of antigen-presenting cell function and induction of immunosuppressive cytokine production may have facilitated additional Demodex infiltration. Usually unapparent/subclinical otherwise.
• Takeaway: UV light for indoor-housed callitrichids should be applied carefully and radiation intensities should be monitored to avoid excessive exposure. Apparent Demodex infestation can be indicative of early immunologically impaired skin function.

Question 54

A recent study described long-term surveillance of langur alphaherpesvirus in a population of silvered langurs.

What zoonotic herpesvirus is langur alphaherpesvirus related to?

How was this discovered? What signs were seen in the langurs?

When is trnsmission at its highest?

What reommendations were made to reduce transmission?

Answer 54

Gustavsen, K. A., Raphael, B. L., Wildes, M. J., McAloose, D., McCann, C. M., Hilliard, J. K., & Calle, P. P. (2018). Long-term surveillance of langur alphaherpesvirus in a zoo population of silvered langurs (trachypithecus cristatus). Journal of Zoo and Wildlife Medicine, 49(2), 345-354.

Abstract:Langur alphaherpesvirus (HVL), a provisionally named alphaherpesvirus in the Simplexvirus genus, was first identified in 1991 at the Bronx Zoo in wild-origin silvered langurs (Trachypithecus cristatus) and their descendants. HVL is closely related to B virus (Macacine alphaherpesvirus 1) based on serologic and genetic data, but its natural history and zoonotic potential remain unknown.A cohort study was undertaken to describe the epidemiology, clinical impact, and potential management implications of this virus in a naturally infected, zoobased population of silvered langurs. Opportunistic surveillance sampling from 1991 through 2015 resulted in 235 serum samples and 225 mucosal swabs from 75 individuals. A total of 43 individuals (57.3%) were seropositive for HVL within this period. Seroprevalence increased significantly with age, and indirect evidence suggested a peak in transmission at the onset of sexual maturity.These findings were similar to the behavior of other simplexviruses in their adapted hosts. Yearly cumulative incidence declined significantly through the study period, with zero or one new case detected each year from 2007 through 2015. The density of this population decreased within the study period for management reasons unrelated to HVL infection, and a change in age distribution or less-frequent contacts may have contributed to low transmission. In addition, clinical signs of simplexvirus infection were rare, and virus isolation was negative on all mucosal swabs, suggesting that viral shedding was infrequent. Yearly period seroprevalence remained relatively constant with a median of 45.8%, likely because of the extended survival of infected individuals within the population.Maintenance of a naturally occurring, novel virus with unknown zoonotic potential in a zoo population for over 25 yr highlights the importance of biosecurity and biosafety for management of silvered langurs and all primate species.

• Alphaherpesviruses in OWP, NWP, GA – simplexviruses can cause inapparent disease, mild mucosal vesicular lesions in natural hosts, or severe systemic disease (Herpes B aka Macacine alphaherpesvirus 1)
• HVL discovered when an animal tested positive for Herpes B after it had bit a staff member – still treated similarly as full zoonotic risk is not known
• 26 of the 43 positive animals remained consistently seropositive
• Three animals with severe oropharyngeal ulceration or fibrinonecrotic plaques did yield isolation of HVL
• Transmission appears to peak during sexual maturity, likely as it is a period of stress – the clinical animals were also in this age range
• Decreasing population density may have reduced the frequency of contacts and potential for transmission
• Removal of langurs just prior to sexual maturity for the SSP may have also decreased their chance of seroconversion
• Primates other than macaques have not been regarded as carriers of potentially zoonotic herpesviruses but should be

Take Home:

• Langur alphaherpesvirus (HVL) is similar to macacine alphaherpesvirus 1 (Herpes B) and was maintained in the population at the Bronx Zoo of 25 years from wild caught individuals. Transmission peaks at sexual maturity.

Question 55

A recent study described the treatment of generalized demodicosis in red-handed tamarins with flurlaner.

What were the clinical sign of these monkeys? How was demodeex confirmed?

What is the mechnism of action of fluralaner?

Answer 55

Churgin, S. M., Lee, F. K., Groenvold, K., Kovi, R. C., Cheung, K. Y., Martelli, P. R., & Zoo, C. (2018). Successful treatment of generalized demodicosis in red-handed tamarins (Saguinus midas) using a single administration of oral fluralaner. Journal of Zoo and Wildlife Medicine, 49(2), 470-474.

Abstract: Two adult sibling red-handed tamarins (Saguinus midas) presented with weight loss and multifocal skin masses. A skin biopsy revealed pyogranulomatous dermatitis with intrafollicular Demodex sp. mites. Subsequent skin scrapes confirmed the presence of live mites within lesions. Initial treatment with topical and oral ivermectin was unsuccessful, and lesions continued to progress. A single dose of fluralaner (Bravecto®, Merck Animal Health, Kenilworth, New Jersey, 07033, USA; 28.125 mg po) was administered to each animal approximately 5 mo after initial presentation. Lesions resolved over the next 3 mo, and all follow-up skin scrapes were negative for both animals. No adverse effects were noted. A single oral administration of fluralaner at 30-35 mg/kg appears adequate and safe for the treatment of generalized demodicosis in red-handed tamarins.

• Discrete hairless nodules on face for several months, bx showed demodex.
• Demodex not considered contagious except Demodex gatoi in cats although seen in these two siblings.
• Fluralaner (Bravecto) – Isoxazoline parasiticide.
  
  • Selective inhibition of arthropod-specific chloride channels.
  • Oral form is flavored, chewable tablet.
  • Once every 12 weeks (25-56 mg/kg depending on size.
• Takeaway: Fluralaner (Bravecto) apparently safe, effective for demodex tx in this spp.

Question 56

A recent study compoared two surgical techniques for sterilization in female marmosets.

Why are gonadal sparing procedures preferred in nonhuman primates?

What were the two techniques described in this study?

What significant differences were there between the two methods?

Answer 56

de Queiroz, F. F., Kristosch, G. C., Soffiati, F. L., Luz, M. J., de Abreu Oliveira, A. L., Borges, T. R. J., … & da Silveira, L. S. (2017). Sterilization of hybrid marmoset (Callithrix sp.) females: An evaluation of two surgical methods. Journal of Zoo and Wildlife Medicine, 48(4), 1095-1101.

Abstract: Population control techniques, either permanent or reversible, are important tools for the management of wildlife in captive and natural environments. Among these, surgical sterilization provides a permanent solution to unwanted reproduction. Surgical techniques can differ in their invasiveness and in the subsequent effect on behavior and physiology. For social animals, techniques that preserve gonads, such as vasectomy for males and ligation of uterine tubes for females, may be preferred because they maintain important physiology that influences behavior. This study compared two sterilization procedures for captive hybrid marmosets (Callithrix sp.). Twenty adult females undergoing tubal ligation were divided into two groups and received treatment either with a laparotomy or a laparoscopic method. The following parameters were evaluated for each female: duration of procedure, pain levels, weight gain, wound healing, adhesion, and inflammation. The results indicate that both techniques were equally effective. However, the conventional surgery may be more advantageous, because it is significantly shorter in duration, is only slightly more invasive, and requires less formal training of the surgeon.

• Ligation of uterine tubes and vasectomy do not alter levels of hormones
  
  • These procedures recommended instead of ovariectomy or orchiectomy given hormonal role in hierarchical relationships of animals
    
    • Primate social behavior is strongly influenced by sex hormones
  • Pomeroy technique - most common uterine sterilization method
    
    • Excision of an ~3cm section of isthmus-ampulla region of uterine tube

Objective - compare two surgical sterilization techniques for wild hybrid callitrichids

• Video-assisted laparoscopic tubal ligation vs conventional tubal ligation
• Compared surgery duration, post-operative pain scores, adhesion, inflammatory response, body weight and behavior

Surgical times varied with the method used, but pain scores, recovery, adhesion incidence, and lesions did not differ between techniques

• Conventional surgery was significantly quicker than laparoscopic method
• Disadvantages of laparoscopy - longer duration of procedure and level of training required of the surgeon

Question 57

A recent study described oronasal squamous cell carcinoma in Francois langurs.

How common is SCC in nonhuman primates?

How effective is treatment?

What relationship between cases did this study find?

What were teh typical clinical signs and lesions in this study?

Are males or females more commonly affected?

Answer 57

Flanders, J. A., Thompson, M. E., Palazzolo, M. J., Garner, M. M., Reed, M., Ialeggio, D. M., … & Gamble, K. C. (2017). ORONASAL SQUAMOUS CELL CARCINOMAS IN FRANÇOIS’LANGURS (TRACHYPITHECUS FRANCOISI). Journal of Zoo and Wildlife Medicine, 48(2), 394-403.

Abstract: Squamous cell carcinomas (SCCs) are common oronasal tumors in nonhuman primates. In this study, 11 cases of oronasal SCC in Franc_ois’ langurs (Trachypithecus francoisi) are described. Five initial cases were discovered on review of the North American Francois’ langur studbook, with a potential familial pattern observed. The studbook was used to identify related individuals, and records were requested for review. Six additional cases were documented, and samples from all cases were submitted for microscopic review, as well as polymerase chain reaction (PCR), immunohistochemistry (IHC), and in situ hybridization (ISH), for generic papillomaviruses and PCR for herpesviruses because either virus may cause SCC in humans and other nonhuman primates. Affected langurs commonly presented with facial swelling or ocular discharge but frequently did not have clinical signs, and carcinomas were diagnosed during routine examinations. Carcinomas were located in the oral or nasal cavities affecting the oral mucosa, tongue, hard palate, or oropharynx. Histologically, SCCs comprised anastomosing cords and nests of neoplastic epithelial cells that differentiated synchronously and asynchronously from peripheral basal type cells to central squamous-type cells and were occasionally oriented around accumulations of necrotic cell debris. Nuclear pleomorphism, anisokaryosis, prominent nucleoli, occasional mitoses, and a scirrhous response were common features. All animals tested negative for both viruses, except two langurs that were positive for generic papillomavirus by PCR, but no papillomavirus was detected by either IHC or ISH. In most cases, affected animals died within 5 mo of diagnosis.

• SCC most common oral neoplasm in nonhuman primates, most commonly in oral cavity
  
  • Baboons and marmosets common with surgical excision unrewarding with most surviving < 7mo
• 5 cases of SCC were noted on review of studbook and 6 more cases identified after close examination
  
  • Immunohistochemistry reviewed by 3 pathologists
  • Additional testing: papilomavirus and herpsevirus PCR, papillomavirus IHC, papillomavirus ISH
    
    • HPV and herpesvirus may cause SCC in humans and other nonhuman primates

All 11 cases had direct genetic relationship to at least one other case = familial pattern

• Median survival time 5mo (range 1wk – 109mo)

Langurs had facial swelling and ocular discharge

• SCC located oral mucosa (5), tongue (4), hard palate (1), and oropharanyx (1)
• Non-keratinizing and basaloid grossly and anastomosing cords and nests of neoplastic epithelial cells to squamous type cells histologically (similar to baboons and marmosets)
• Slow growing, locally invasive
• Metastasis to regional LN and lung (36.4%)

Striking resemblance to SCC in humans in location, histology, behavior, and prognosis

• Males more commonly affected in langurs in this study (same seen in humans)

Differences from human SCC:

• NO evidence of herpesvirus or papillomavirus to cause SCC

Take home: SCC common malignancy in Francois langurs, slow growing, locally invasive, with no underlying viral cause

Question 58

A recent study evaluated the use of serology to diagnoses baylisascaris in nonhuman primates.

How common were positive primates identified?

This test didn’t work well in which groups of primates?

Were there any differences based on diet type?

Describe the basic life cycle and pathogenesis of baylisascaris infestation.

Answer 58

Zimmerman, D. M., Dangoudoubiyam, S., & Kazacos, K. R. (2019). Serological diagnosis of baylisascaris procyonis in primates using a human elisa test. Journal of Zoo and Wildlife Medicine, 50(2), 414-420.

Abstract: The usefulness of a human enzyme-linked immunosorbent assay (ELISA) for serological diagnosis of Baylisascaris procyonis larva migrans was assessed in nonhuman primates (NHP). The test was originally developed as an assay performed on human samples at Purdue University. Six participating zoos submitted 258 NHP serum samples, spanning these major phylogenetic groups: 1) great apes (n ¼ 84), 2) lesser apes (n ¼ 17), 3) Old World monkeys (n ¼ 84), 4) New World monkeys (n ¼ 20), and 5) prosimians (n ¼ 53). Sera were tested in duplicate using a microtiter-well ELISA with B. procyonis larval excretory-secretory proteins as antigen, and serum from an experimentally infected baboon (Papio anubis) served as positive control. The ELISA clearly identified seropositive animals in all zoos. With putative cutoffs of optical density (OD) measured at 405 nm (OD405) of <0.150= negative, 0.150–0.250= indeterminate, and .0.250 = positive, 149 of 258 (57.8%) were clearly negative (mean OD 0.046), and 78 of 258 (30.2%) were clearly positive (mean OD 0.657, range 0.253–1.773), the rest being indeterminate. Of these, 15 were high positive with OD 1.095–1.773 (mean 1.314). Positive animals were seen from all zoos; 76 (97.4%) were great apes, lesser apes, or Old World monkeys. The four highest ODs were in a siamang (Symphalangus syndactylus), lion-tailed macaque (Macaca silenus), Sumatran orangutan (Pongo abelii), and western lowland gorilla (Gorilla gorilla gorilla), all from different zoos. Prosimians had a mean OD of 0.039 and New World monkeys 0.021, indicating that human reagents either did not work for these groups or few infected animals were represented. These results indicate that the human ELISA for B. procyonis works well for at least higher phylogeny NHP and that serologic evidence of infection is surprisingly common, correlating with what is known for exposure to this parasite in zoos.

• Increasingly recognized helminthic disease🡪 larval migrans, often to CNS.
• Risk of infection thought to be greater than recognized. Raccoon is end host
• Baylisascaris eggs resistant in environment and infective in soil for years
  
  • In zoos found in stored hay and straw, stored grain/food items, sidewalks, within enclosures
• Well recognized zoonosis, difficult to diagnose clinically
  
  • Eggs are not shed in paratenic hosts, so cannot diagnose by fecal exam
  • CSF fluid may have eosinophilic pleocytosis
  • Advanced imaging often unrearding, sometimes seen as lesions in deep white matter on MRI
  • Diagnosis currently dependent on finding anti-B. procyonis ATB in serum and CSF
  • PCR can miss it, may be more useful post-mortem
• ELISA made for Baylisascaris in humans used as a screening test and in clinical cases using products from L3 larvae

STUDY DESIGN: Sera from individuals banked or prospectively from animals with CS of Baylisascaris neural larval migrans tested using ELISA- from 6 different zoos

• Positive animals seen at all zoos; 97% were great apes, lesser apes or old World monkeys
• Older animals (30+) had higher OD’s; no difference in genders
• 44% of folivores were positive
• Animals with highest OD were not clinically affected at time of sampling; animals with clinical signs were more likely to be seropositive

DISCUSSION:

• At least 31 NHP species have been identified with proven or suspect4ed Bayliascarlis NLM
• Prosimians and New World Monkeys had lower mean OD’s- possible that human reagents didn’t work for the “lower” primate groups or too few infected aniamls represented
• Human positives 1.3-3.2 OD ranges- no “high” range found in this study in NWP
  
  • Experimentally infected baboon with fatal NLM had OD range 1.1-1.3
• Widespread exposure to B. procyonis for other animals and people
• Older animals had higher ODs- in humans, positive reactivity also increased with age
• Seroprevalence varied from 14-055% across the 6 zoos
  
  • Strictly arboreal species may be less likely to encounter raccoon feces
  • Husbandry changes may be able to ameliorate many infections
• No significant difference observed between frugivores and folivores, insectivores or omnivores
• Animals with clinical signs more likely to be seropositive, though animal with highest OD was asymptomatic (this is very typical in humans too)
• Larvae are not neurotropic, but will sometimes enter CNS (5-7%) as a result of dissemination
  
  • Interpret results with caution in light of clinical findings and history
• ELISA in this study detected immunoglobulin G antibodies, which just signifies prior infection

TAKE HOME: Common to have serologic evidence of Bayliascaris infection in zoos. Human ELISA works well in higher phylogeny NHP but must be interpreted with caution. Zoos should take appropriate action to protect NHPs.s

Question 59

A recent study validated an ELISA to quantify alpha-1 proteinase inhibitor (A1-P1) concentrations in marmoset serum and feces.

What is marmoset wasting syndrome?

How is enteric protein loss best quantified?

Why is alpha-1 proteinase inhibitor a useful protein to measure?

Answer 59

Parambeth, J. C., Lidbury, J. A., Suchodolski, J. S., & Steiner, J. M. (2019). Development and analytic validation of a sandwich ELISA for the measurement of α1-proteinase inhibitor concentrations in serum and feces of common marmosets (Callithrix jacchus). American journal of veterinary research, 80(3), 259-264.

ABSTRACT:

• OBJECTIVE To develop and validate a sandwich ELISA for the measurement of α1-proteinase inhibitor (α1-PI) concentrations in serum and fecal samples obtained from common marmosets (Callithrix jacchus).
• SAMPLE Leftover serum (n = 42) and fecal (23) samples submitted for diagnostic testing; paired serum and fecal samples obtained from 30 common marmosets at 2 research colonies.
• PROCEDURES A sandwich ELISA was developed and analytically validated by determining the lower limit of detection, linearity, accuracy, precision, and reproducibility. Reference intervals for α1-PI concentrations in serum and feces of common marmosets were calculated.
• RESULTS The standard curve was generated for concentrations between 1 and 100 ng/mL. Mean ± SD observed-to-expected ratio for serial dilutions of serum and fecal samples was 117.1 ± 5.6% (range, 112.2% to 123.0%) and 106.1 ± 19.7% (range, 82.6% to 130.2%), respectively. Mean observed-to-expected ratio for spiking recovery of serum and fecal samples was 102.9 ± 12.1% (range, 86.8% to 115.8%) and 97.9 ± 19.0% (range, 83.0% to 125.1%), respectively. Reference interval for serum concentrations of α1-PI was 1,254 to 1,813 µg/mL, for 3-day mean fecal concentrations was 11.5 to 42.2 µg/g of feces, and for 3-day maximum fecal concentrations was 13.2 to 51.2 µg/g of feces.
• CONCLUSIONS AND CLINICAL RELEVANCE The ELISA was linear, accurate, precise, and reproducible for quantification of α1-PI concentrations in serum and feces of common marmosets. However, the ELISA had limited linearity and accuracy for spiking recovery of fecal samples. (Am J Vet Res 2019;80:259–264)

Key Points

• GI tract inflammation commonly seen in marmoset colonies, with unknown etiology
• Clinical signs include diarrhea, progressive weight loss despite good appetite, failure to thrive, anemia, hypoproteinemia
• Suspected to be variant of IBD
• Currently called CLE, but previously described as marmoset wasting syndrome and bone and GI disease of marmosets
• Diagnosis at necropsy common
• Excretion of 51 Cr-albumin in feces is the test of choice for detecting enteric protein loss but is difficult to test for
  
  • A1 proteinase inhibitor is lose in the GI tract at a rate similar to albumin and can be detected with ELISA

STUDY DESIGN: Used leftover serum and fecal samples from euthanized marmosets at diagnostic lab to create ELISA and for detecting normal reference ranges. Fecals collected over 3 days.

• Standard curves were reproducible; lower detection limit of the assay was 0.006ug/L
• Calculated dilutional parallelism and spiking recovery for observed:expected values for fecal and serum values
• Reference intervals: Calculated 3day mean and 3day max concentrations for fecals as well as RI for serum a1-PI concentrations.
• Precise and reproducible ELISA assay developed for both serum and fecal samples in marmosets
• Limitations included mild deviations from generally accepted O:E ranges for dilutional parallelism and spiking recovery in serum; more pronounced in fecal samples
• Underestimated a1-PI when expected concentration was less than 2ng/g feces, but should not be clinically relevant
• The reference interval for concentrations of α1-PI in serum of marmosets was 1,254 to 1,813 µg/ mL, which is comparable to dogs and cats
• Fecal α1-PI concentrations were much higher for the 30 healthy marmosets of the study reported here; they ranged from 11.4 to 48 µg/g of feces (median, 27.1 µg/g of feces) on day 1- higher than dogs and cats. Considerable variation amongst all 3 days of feces collected
• Limited by sample size (reference interval should use 120 animals, not 30). Unknown effects of storage of samples in freezer

TAKE HOME: Developed an ELISA for quantification of a1-PI in serum and fecal extracts from marmosets.

Question 60

A recent study compared ultrasonography and computed tomography to evaluate kidney and adrenal gland size in Callimicos.

How well did US and CT agree?

Kidney size best correlated with what value?

Were there any correlations with biochemistry values?

Answer 60

James Johnson III, Jennifer Langan, Sathya K. Chinnadurai, Randi Dress, Mark Warneke, Matthew Allender. Comparison of transcutaneous ultrasound and computed tomography evaluation of kidney size and evaluation of adrenal gland size using ultrasound in a colony of Callimicos (Callimico goeldii). JZWM 2018 49(4): 887 –892

ABSTRACT: Both kidney and adrenal gland disease have been identified in callimicos (Callimico goeldii). Ultrasonography (US) and computed tomography (CT) are routinely utilized in veterinary patients with suspected renal or adrenal disease to determine size, shape, and echogenicity of these organs. No previous US and CT kidney and adrenal gland measurements have been published for callimicos. In this study, 14 callimicos were anesthetized using isoflurane via facemask to evaluate kidney and adrenal gland size using US for both organs and CT for kidneys. Animals were considered clinically healthy based on history, physical examination, hematology, serum chemistry, urinalysis, and abdominal US. Ultrasound organ measurements for length (L), width (W), and height (H) in centimeters (mean/median, 95% confidence interval) in clinically healthy animals were right kidney (L = 1.90, 1.76-2.01; W = 1.05, 0.97-1.13; H = 1.59, 1.48-1.69), left kidney (L = 1.84, 1.72-1.95; W = 1.16, 1.04-1.28; H = 1.54, 1.43-1.65), right adrenal gland (L = 0.38, 0.33-0.57; H = 0.19, 0.15-0.31) and left adrenal gland (L = 0.36, 0.32-0.39; H = 0.18, 0.17-0.20). All kidney measurements were positively correlated with animal weight ( P < 0.05) but had no significant correlation to age. Measurements did not have any significant relationship to evaluated blood and urine parameters. Results from this study establish baseline measurements for callimico kidneys and adrenal glands to help clinicians use these imaging modalities for evaluation of these organs in this endangered species.

• Kidney and adrenal gland pathology have been identified in Callimicos but etiology remains uncertain
• Aim to report baseline data for kidney and adrenal gland measurements using ultrasound and CT
• 14 animals used in study
• Good agreement between CT and ultrasound
• Kidney measurements
  
  • Right and left kidney similar, except left kidney were wider
  • Positively correlated with animal weight except kidney height
  • No difference between sexes
  • Not correlated with hematology, serum chemistry, or urinalysis
    
    • May be due to healthy animals being evaluated
    • Changes correlated with bloodwork changes in dogs, cats, and humans

Adrenal gland measurements

• No difference between sexes
• No correlation between adrenal size and weight

Take home: Ultrasound and CT have good agreement for kidney and adrenal measurements, first study evaluating measurements. No correlation of adrenal measurements and animal size/weight. Positive correlation with kidney measurements with animal size.

Question 61

A recent study described Yersinia pseudotuberculosis infections within primates, artiodactyls, and birds within a zoological facility in the UK.

How is yersinia transmitted?

What are the typical clinical signs? Do they vary by species?

What is a potential predisposing factor?

Describe treatment of yersiniosis.

What are some common lesions?

Answer 61

Ceccolini, M. E., Macgregor, S. K., Spiro, S., Irving, J., Hedley, J., Williams, J., & Guthrie, A. (2020). Yersinia pseudotuberculosis infections in primates, artiodactyls, and birds within a zoological facility in the United Kingdom. Journal of Zoo and Wildlife Medicine, 51(3), 527-538.

Infection with Yersinia pseudotuberculosis can be difficult to diagnose and treat successfully. Twenty-four cases from the Zoological Society of London (ZSL) London Zoo and ZSL Whipsnade Zoo were identified between 2001 and 2019. Husbandry, medical, and postmortem records for six primates, 10 artiodactyls, and eight birds were reviewed to identify common clinical signs and gross lesions. Most cases occurred during the winter; however, an outbreak in four primates occurred during the summer following a period of stress associated with increased ambient noise and activity. Common clinical signs included lethargy (6/6 primates, 4/10 artiodactyls, 4/8 birds) or death without premonitory signs (3/10 artiodactyls, 4/8 birds). Once clinical signs were observed, disease progressed quickly. Poor condition was common in mammals (6/6 primates, 9/10 artiodactyls), but often went undetected until postmortem examination. Neurological signs occurred in three of six primates. Diarrhea and anorexia were uncommon in all animals. Hepatitis was observed in all groups (4/6 primates, 2/10 artiodactyls, 4/8 birds), mesenteric lymphadenomegaly was common in mammals (4/6 primates, 8/10 artiodactyls), and gastroenteritis was common in artiodactyls (7/10). Erythematous, punctate rashes, which have only been reported with yersiniosis in humans, were present in three of six primates. Bacterial cultures from the liver in primates and birds or enlarged mesenteric lymph nodes in artiodactyls were often diagnostic. All isolates were susceptible to marbofloxacin, oxytetracycline, streptomycin, ceftazidime, amoxicillin clavulanic acid, trimethoprim sulfamethoxazole, azithromycin, and doxycycline, and resistant to clindamycin. Histopathology and Perl’s Prussian blue stains were performed on available liver samples (n = 18). Intracellular hemosiderin was present in 17 of 18 cases. Additional research is needed to determine if there is a relationship between hemosiderosis and yersiniosis.

• Yersinia pseudotuberculosis - zoonotic, gram-negative, facultative, anaerobic coccobacillus, ubiquitous, 14 serotypes (not host-specific)
  
  • Psychrophile (prefers 4-20C, survives as low as -20C)
  • Wild rodents and bird reservoirs - transmission fecal oral (contaminated water/food)
  • Sporadic to epizootic
• CS: lethargy, hyporexia, dehydration, poor condition, diarrhea, abortion, peracute death with not premonitory signs
  
  • Subclinical cases documented in cervids, primates, carnivores, rodents, and birds
  • Pathogenicity related to host immunocompetency, virulence factors, environmental conditions (cold, wet weather)
  • Availability of excess iron believed to promote growth - hemosiderosis associated with increased susceptibility in humans, mice, and birds
  • Mammals: often primary GI disease (ulcerative enteritis, mesenteric lymphadenomegaly, and hepatitis)
  • Birds: lymphoreticular, hepatitis, splenitis
• Diagnosis: culture, PCR on feces, serum, or tissues, growth often suppressed by GI bacteria, can improve with cold enrichment, can take up to 6 weeks

Key Points

• Post-mortem records, histopath on archived liver samples in formalin, PPB stain for hemosiderosis, culture and gram stain from archived isolates
• 6 primates: white-faced saki monkey, silvery marmosets
  
  • Cluster in August, housed together, underconditioned, next to construction
  • Acute death within 24 hours or lethargy, ataxia, paraplegia, hyporexia and death in 5-9 days
  • Multifocal nodular abscesses in livers, lung, enlarged mesenteric lymph nodes, petechial hemorrhages in skin, GI
  • Yptb isolated from liver, heart, brain, kidney, spleen, lung, GI, feces
• 10 artiodactyls: Chinese water deer, axis deer, fallow deer, gemsbok, impala, scimitar-horned oryx
  
  • Death within 24 hr, poor BCS, lethargy, diarrhea, enlarged mesenteric lymph nodes, hemorrhage in GI, necrotizing gastroenteritis, hepatic abscesses, some comorbidities
  • Yptb isolated from mesenteric lymph nodes, liver, abdomen, spleen, GI, heart, pharyngeal abscess, and feces
• 8 birds: toco toucan, Fisher’s turacos, Von der Decken’s hornbill, Sulawesi hornbill, tarictic hornbills
  
  • Acute death within 24 hours, 1 case survived 3 days.
  • Hepatic abscesses, splenomegaly +/- nodules and necrosis, effusion, nodules in air sacs, bacterial colonies visible in multiple organs
  • Yptb isolated from liver, spleen, lung, choana, coelom, cloaca, heart, and feces
• Various treatment attempted: TMS, meloxicam, Clavamox, marbofloxacin single dose, long-acting oxytetracycline, doxycycline
  
  • Asymptomatic conspecifics moved to a new enclosure and treated remained clinically normal
  • Some animals died up to 6 weeks after finishing antibiotic courses
  • Antibiotics may have been discontinued prior to resolution or infection or continued exposure, insufficient plasma antimicrobial levels, or inadequate tissue penetration
• All isolates in the study were susceptible to marbofloxacin, oxytetracycline, streptomycin, ceftazidime, clavamox, and TMS
  
  • All isolates were resistant to clindamycin
• Hemosiderosis may have predisposed animals to yersiniosis (positive in 94% of cases) or developed secondary to hepatic injury by Yptb
• Most cases during late autumn, winter, early spring, cold and rainy, sporadic and associated with stressors, poor condition, or comorbidities
• Atypical findings: absence of gross GI ulceration in all cases, neurologic signs and dermal hemorrhages in primates
• Isolation from feces was rarely successful in primates, but was successful in birds

Conclusions

• Yersiniosis should be treated early, with appropriate antibiotics, and for an extended period
• Immunosuppression from env stressors including inclement weather is a risk factor
• Hepatic hemosiderosis was common in affected animals
• Poor condition, lethargy, and death without premonitory signs was frequent, diarrhea and anorexia were not commonly observed.
• Most animals died or were euthanized within 24 hr of onset of clinical signs
• Gross hepatic abscesses and mesenteric lymphadenopathy should increase suspicion, absence of ulcerative enteritis should not rule it out
• Culture from liver in primates and birds or enlarged lymph nodes in artiodactyls were diagnostic
• Fecal cultures should be considered for surveillance in birds

Question 62

A recent study compared FM, FMidK, and KMed anesthetic protocols in Japanese macaques.

Answer 62

JZWM 2018 49(1) 99–107

COMPARISON OF INTRAMUSCULAR FENTANYL-MIDAZOLAM, FENTANYL-MIDAZOLAM-KETAMINE, AND KETAMINEMEDETOMIDINE FOR IMMOBILIZATION OF JAPANESE MACAQUES (MACACA FUSCATA)

Rolf-Arne Ølberg, D.V.M., D.V.Sc.,Melissa Sinclair, D.V.Sc., Dipl. A.C.V.A.A., Ian K. Barker, D.V.M., Ph.D., and Graham Crawshaw, B.Vet.Med., Dipl. A.C.Z.M.

Abstract: The combination of fentanyl and midazolam is commonly used as a sedative in humans. The objective of this study was to evaluate the sedative properties and physiological effects of fentanyl-midazolam and fentanyl-midazolam-ketamine compared with medetomidine-ketamine given intramuscularly in Japanese macaques (Macaca fuscata). In a randomized crossover design, eight Japanese macaques were hand-injected with either 30 lg/kg fentanyl þ 0.3 mg/kg midazolam (FM), 15 lg/kg fentanyl þ 0.3 mg/kg midazolam þ 5.0 mg/kg ketamine (FMK), or 0.05 mg/kg medetomidineþ5.0 mg/kg ketamine (MedK). Heart rate; indirect systolic, mean, and diastolic arterial pressure; respiratory rate; blood gas concentrations; rectal temperature; and duration of immobilization were recorded. Mixed linear models were used to evaluate the effects of drug treatment on all continuous variables, with a significance level of P , 0.05. Only three of seven animals receiving FM were successfully immobilized. All eight animals in both the FMK and MedK treatment groups had a rapid, smooth induction and were successfully immobilized. Both FMK and MedK treatments resulted in significant hypoxia and the animals required supplemental oxygen via face mask. The mean duration of FMK immobilization was 42 +/- 10 min, significantly shorter than the 65 6 14 min for the animals receiving MedK. Immobilization with MedK resulted in significantly lower heart rates, and significantly higher arterial pressure compared with FMK. Hypoventilation was significantly more pronounced in FMK-treated animals compared with MedK treatments. Immobilization with FMK resulted in a gradual, slow recovery whereas MedK-treated animals woke up more rapidly. Fentanyl-midazolam alone is not a useful sedative in Japanese macaques. A combination of fentanyl and midazolam with ketamine can be used as an alternative to medetomidine-ketamine in this species.

Key words:

• Medetomidine-ketamine is recommended for immobilization of primates by several authors
• Compared fentanyl-midazolam and fentanyl-midazolam-ketamine with medetomidine-ketamine
• FM
  
  • 3 out of 7 animals were NOT immobilized = not useful in this species
    
    • Responded to sudden movement, noise, and blood sampling
  • Highest HR values

FMK and MedK

• Both all animals successfully immobilized
• FMK slightly longer induction time likely related to slow onset of midazolam effects
• FMK hypoventaliation more pronounced than MedK
  
  • Both hypoxemia while breathing room air
• FMK shorter mean duration (42 +/- 10min) than MedK (65 +/- 14 min)
• MedK lower HR (likely secondary to medetomidine) and higher arterial pressure than FMK
• MedK more rapid recovery than FMK (slow, gradual recovery)
  
  • No premonitory change in physiologic parameters, a potential hazard when working with a dangerous species

FMK can be used as an alternative to MK with the advantage of more predictable recovery BUT results in more severe hypoventilation

Take home: FM is inadequate for immobilization while FMK can be used as an alternative to MK with the advantage of more predictable recovery BUT results in more severe hypoventilation

Question 63

A recent study compared FM, FMK, and KMed anesthetic protocols in Japanese macaques.

Which protocol was least likely to produce adequate sedation?

Which produced rapid inductions? Which produced rapid recoveries?

Which produced the most hypoventilation? Which produced the lower heart rate and BP?

Answer 63

JZWM 2018 49(1) 99–107

COMPARISON OF INTRAMUSCULAR FENTANYL-MIDAZOLAM, FENTANYL-MIDAZOLAM-KETAMINE, AND KETAMINEMEDETOMIDINE FOR IMMOBILIZATION OF JAPANESE MACAQUES (MACACA FUSCATA)

Rolf-Arne Ølberg, D.V.M., D.V.Sc.,Melissa Sinclair, D.V.Sc., Dipl. A.C.V.A.A., Ian K. Barker, D.V.M., Ph.D., and Graham Crawshaw, B.Vet.Med., Dipl. A.C.Z.M.

Abstract: The combination of fentanyl and midazolam is commonly used as a sedative in humans. The objective of this study was to evaluate the sedative properties and physiological effects of fentanyl-midazolam and fentanyl-midazolam-ketamine compared with medetomidine-ketamine given intramuscularly in Japanese macaques (Macaca fuscata). In a randomized crossover design, eight Japanese macaques were hand-injected with either 30 lg/kg fentanyl þ 0.3 mg/kg midazolam (FM), 15 lg/kg fentanyl þ 0.3 mg/kg midazolam þ 5.0 mg/kg ketamine (FMK), or 0.05 mg/kg medetomidineþ5.0 mg/kg ketamine (MedK). Heart rate; indirect systolic, mean, and diastolic arterial pressure; respiratory rate; blood gas concentrations; rectal temperature; and duration of immobilization were recorded. Mixed linear models were used to evaluate the effects of drug treatment on all continuous variables, with a significance level of P , 0.05. Only three of seven animals receiving FM were successfully immobilized. All eight animals in both the FMK and MedK treatment groups had a rapid, smooth induction and were successfully immobilized. Both FMK and MedK treatments resulted in significant hypoxia and the animals required supplemental oxygen via face mask. The mean duration of FMK immobilization was 42 +/- 10 min, significantly shorter than the 65 6 14 min for the animals receiving MedK. Immobilization with MedK resulted in significantly lower heart rates, and significantly higher arterial pressure compared with FMK. Hypoventilation was significantly more pronounced in FMK-treated animals compared with MedK treatments. Immobilization with FMK resulted in a gradual, slow recovery whereas MedK-treated animals woke up more rapidly. Fentanyl-midazolam alone is not a useful sedative in Japanese macaques. A combination of fentanyl and midazolam with ketamine can be used as an alternative to medetomidine-ketamine in this species.

Key words:

• Medetomidine-ketamine is recommended for immobilization of primates by several authors
• Compared fentanyl-midazolam and fentanyl-midazolam-ketamine with medetomidine-ketamine
• FM
  
  • 3 out of 7 animals were NOT immobilized = not useful in this species
    
    • Responded to sudden movement, noise, and blood sampling
  • Highest HR values

FMK and MedK

• Both all animals successfully immobilized
• FMK slightly longer induction time likely related to slow onset of midazolam effects
• FMK hypoventaliation more pronounced than MedK
  
  • Both hypoxemia while breathing room air
• FMK shorter mean duration (42 +/- 10min) than MedK (65 +/- 14 min)
• MedK lower HR (likely secondary to medetomidine) and higher arterial pressure than FMK
• MedK more rapid recovery than FMK (slow, gradual recovery)
  
  • No premonitory change in physiologic parameters, a potential hazard when working with a dangerous species

FMK can be used as an alternative to MK with the advantage of more predictable recovery BUT results in more severe hypoventilation

Take home: FM is inadequate for immobilization while FMK can be used as an alternative to MK with the advantage of more predictable recovery BUT results in more severe hypoventilation

Question 64

A recent report described cysticercosis in a Nilgiri Langur.

What is the etiologic agent of Cysticercus? What are the typical definitive and intermediate hosts?

Answer 64

Bleyer, Martina, Risch, Tina, Roos, Christian, Kaup, Franz- Josef, and Mätz-Rensing, Kerstin. Taenia Crassiceps cycticercosis in a Nilgiri Langur (Semnopithecus johnii). JZWM 49 (2) 501-504.

Abstract: A captive-born adult female Nilgiri langur (Semnopithecus johnii) developed an edematous swelling of the left thigh and a firm mass around the right ankle joint. The animal also suffered from lethargy and anorexia and was euthanized because of poor general condition. Necropsy revealed that the skeletal muscle of the left thigh had been replaced by a multilocular cystic mass containing numerous sand-grain–sized whitish structures. Small cysts were also present in the lung and the myocardium. The mass of the right ankle joint was histologically consistent with a myxosarcoma. In contrast, the cystic masses from the left thigh, the lung, and the myocardium represented metacestode tissue with evidence of numerous larval cestodes consistent with cysticerci. Cysticerci showed morphological characteristics of Cysticercus longicollis, the larval form of Taenia crassiceps, which was confirmed by genetic analysis. This is the first documented case of a Taenia crassiceps cysticercosis in an Old World monkey species.

• Nilgiri langur developed edematous swelling of thigh and firm mass of ankle
• Ankle mass = myxosarcoma
• Muscular, pulmonary, and myocardial cystic lesions of metacestode tissue
  
  • Cystic mass with sand size white structures replacing thigh skeletal muscle
  • →Cysticercus longicollis – larval form Taenia crassiceps
• Sword-shaped rostellar hooks with long “blade” and short “handle” = distinctive feature of Cysticercus longicollis
• Taenia crassisceps is cestode parasite of Norther hemisphere
  
  • Canids definitive host – most commonly Red fox in Europe and Artic fox + Red fox in NA
  • Rodent species and rabbits intermediate hosts – most common Common vole in Europe
  • Proliferate by exogenous and endogenous budding (in contrast to other Taneia)
• Previous reports in lemurs
• Likely source of infection in this case is tapeworm carrying dog/cat or fox feces or contaminated vegetables

Take home: First report of Taenia crassiceps cystercosis in old world monkey species. Present in skeletal muscle, heart, and lung.

Question 66

A recent study described the transmission of Pterygodermatitis nycticebi in a colony of Goeldi’s monkeys.

What type of organism is Ptrygodermatites nycticebi? How is it diagnosed?

How did this monkeys present?

What treatments were used? Were any effective?

What are some potential intermediate hosts?

Answer 66

Annina Balsiger, Karin Federer, Felix Grimm, Dr. phil.II, and Peter Deplazes. Transmission of Pterygodermatites nycticebi in a colony of Goeldi’s monkeys (Callimico goeldii) and evaluation of treatment and control. JZWM 2018 49(4) 893–901

Abstract: Over a 2-yr period, four Goeldi’s monkeys (Callimico goeldii) died in a private zoo due to infections with the spirurid nematode Pterygodermatites nycticebi. Therapeutic measures with different anthelmintics were not successful. Due to the severe consequences caused by these infections, different actions were initiated, including sanitation measures and controlling of potential intermediate hosts (coprophagous arthropods). To identify possible intermediate hosts, arthropod species detected in the enclosure—parasite-free German cockroaches (Blattella germanica), European earwigs (Forficula auricularia), and rough woodlice (Porcellio scaber)—were experimentally fed with feces of monkeys with patent P. nycticebi infections, resulting in established infections with third-stage larvae (L3) in roaches and earwigs. Furthermore, spiruroid L3 were detectable in 43% of the roaches and 30% of earwigs caught at the zoo. Polymerase chain reaction and sequence analysis of eggs, larval, and adult stages resulted in identical results, confirming the establishment of the parasite’s life cycle in the zoo. This is the first documentation of the vector capacity of the European earwigs for P. nycticebi. As a measure of sanitation, a large part of the enclosure was emptied and cleaned. The Goeldi’s monkeys were quarantined and treated with levamisole (7.5 mg/kg sc twice in intervals of 2 wk). Repeated coprologic examinations by zinc chloride flotation were undertaken. After the levamisole therapy, eggs were not found in the feces for 3 mo. However, shortly after resettling the monkeys into the sanitized enclosure, reshedding of small amounts of spirurid eggs was observed, whereupon deworming with levamisole was prescribed several times per year. The sanitation measures and the elimination of the intermediate hosts in a natural enclosure are presented as an example of the long-term controlling of the parasites.

Key points:

• Pterygodermatites nycticebi parasitizes intestinal tract causing high morbidity but low mortality (diarrhea, cachexic, weak)
  
  • Diagnosis by thick shelled embryonated eggs
  • Specific gravity of eggs is high, only float in high density media 🡪 egg excretion can be overlooked
  • Egg detection not possible during prepatent period
• Study design
  
  • Case report on 4 Goeldi’s monkeys that died from pterygodermitites nycticebi
  • Nematode development in possible intermediate hosts
    
    • German cockroaches and European ear wigs caught in enclosure and examined for nematode larvae
    • Diet mealworms and crickets examined for nematode larvae

Case report

• Goeldi’s monkeys live with American alligators, alligator snapping turtles, and red-footed tortoises AND in close proximity to agoutis, owl monkeys, pygmy marmosets
• 4 monkeys died weakness and diarrhea 🡪 necrotizing colitis, worm granulomas on necropsy
• Fenbendazole and selamectin 🡪 NO reduction in egg excretion
• Doramectin 🡪 no eggs for 3 weeks
• Levamisole 🡪 no eggs for over 3 months
• Positive for eggs 2 weeks post returning to enclosure 🡪 decision to regularly deworm with levamisole 3-4 times yearly 🡪 no eggs detected or losses since then

Agouti, owl monkeys, and pygmy marmosets NOT infected, negative for eggs

German cockroaches, European ear wigs, rough wood lice fed contaminated monkey feces

• Nematode larvae in experimentally infected cockroaches and earwigs
• Could not infect woodlice

German cockroaches, European ear wigs, and mice caught in enclosure

• Nematode larvae in cockroaches and earwigs
• No nematode stages in mice

No parasite stages found in feeder insects (mealworms and crickets)

Discussion

• Cockroaches and earwigs might be intermediate hosts – vector competence confirmed
• Complete earwig elimination proved impossible
• Since 2 weeks not enough for prepatency period 🡪 likely Levimasole did not completely eliminate worms and merely suppressed egg excretion
• Recommendations
  
  • Levimasole treatment 3-4 times yearly
  • Twice yearly corprological testing recommended
  • Regular disinfections of inner compounds

Take home: Pterygodermatities nycticebi lead to mortality in Goeldi’s monkeys, Levimasole suppressed egg excretion but did not eliminate worms, Levimasole treatment 3-4 times yearly successful at suppressing egg excretion

Question 67

A recent study described noninvasive sampling of primates in Peru.

What method did they use?

Which demographic of primates was more likely to chew?

How useful were the samples obtained?

Where there any potential adverse effects?

Answer 67

Optimizing a Noninvasive Oral Sampling Technique for Semicaptive Neotropical Primates in Peru

JWD 2020 56(1): 192-196 – Short communication

Darby McDermott, A. Patricia Mendoza, Tierra Smiley-Evans, Milagros Zavaleta, Akram A. Da’Dara, Jorge O. Alarco ́n, Raul Bello, Paola Santa Vidal, and Marieke Rosenbaum

ABSTRACT: Disease surveillance in Neotropical primates (NP) is limited by the difficulties associated with anesthetizing NP for sample collection in remote settings. Our objective was to optimize a noninvasive method of oral sampling from semicaptive NP in Peru. We offered 40 NP at Taricaya Rescue Centre in Madre de Dios, Peru ropes coated in various attractants and measured variables (acceptance of the rope, chewing time, and volume of fluid eluted from ropes) that may affect sample acquisition and quality. We preserved samples by direct freezing in liquid nitrogen or by storing samples in RNA stabilization reagent at room temperature. Sample integrity was measured by testing for mammalian cytochrome b with the use of conventional PCR. The NP successfully chewed on a rope in 82% (125/152) of trials. Overall sample integrity was high, with 96% (44/46) of samples (both directly frozen and stored in stabilization reagent) testing positive for cytochrome b. The number of times that an individual NP was exposed to the rope procedure and NP age were associated with higher acceptance rates and the NP successfully chewing on the rope. We conclude that ropes serve as a feasible noninvasive method of obtaining oral samples from NP at rescue centers and could be used in future studies to evaluate population genetics and for pathogen surveillance for population health monitoring.

• Noninvasive method using sterile ropes covered in jam was developed to collect samples from Old World primates
  
  • has not been used in neotropical primates
• N = 152 trials using 40 neotropical primates (NP)
  
  • Swabs attached to nylon string coated in guava paste, strawberry jam, or mashed banana
  • Each attractant offered 2-3 times to NP
• 82% chewed on ropes
  
  • Adults 4.0 times more likely to chew than juveniles
  • NP exposed to the rope methods four or more times were 7.6 times more likely to chew
• No significant difference between attractant type 🡪 all three suitable for use
• Ropes was effective and behaviorally acceptable technique to collect oral samples
  
  • High sample integrity with 96% tested positive for mammalian cytochrome b
    
    • 2 negative samples (both Lagothrix) likely due to primer having no target
  • 3 consumed the rope
    
    • Potential behavior difference as did not occur with old world primates

Individual sampling difficult as NP frequently shared ropes with other NP

Take home: non-invasive rope oral sampling technique is effective and behaviorally acceptable

References: none

Question 68

A recent study established the hematologic and biochemical reference values for Panamanian White-Faced Capuchins in Costa Rica.

What erythrocyte morphology was commonly observed?

Answer 68

Hematology and Serum Biochemistry Values of Healthy Free-ranging Panamanian White-faced Capuchins (Cebus imitator) in Costa Rica

JWD 2020 56(1): 229-233 – Letter

Sof ́ıa Bernal-Valle, Mauricio Jime ́nez-Soto, and Ana Meneses-Guevara

ABSTRACT: We describe the hematology and serum biochemistry values for 26 free-ranging Panamanian white-faced capuchins (Cebus imitator) in Costa Rica. Howell-Jolly bodies and microfilariae were observed in some animals. This baseline information is a tool for health assessment and species conservation.

• No data for wild Costa Rican Panamanian white- faced capuchins and only a single study for captive animals
• N = 26 wild capuchins, captured using darts or blowgun
• Hematology showed higher dispersion than leukogram
  
  • Leukocytes are more responsive to proximate conditions than erythrocytes
• No cell morphology changes
• Howell-Jolly bodies in 35% of erythrocytes 🡪 common in NH primates
• Microfilaria in 4 animals without clinical signs
• Hematology and serum biochemistry results were within the ranges reported for Cebus spp.

Take home: hematology and serum biochemistry values for free-ranging white-faced capuchins

Reference: none

Question 69

A recent study investigted the Leptospira status of primates and rodents at a zoo in Colombia.

What prevalent was lepto seropositivity in the rodents and primates?

Were any positive on PCR or culture?

Answer 69

Woolf, Danielle, et al. “Leptospira species status of captive nonhuman primates and free-ranging rodents at the barranquilla zoo, colombia, 2013.” Journal of Zoo and Wildlife Medicine 51.4 (2021): 780-788.

Abstract: Leptospirosis is a zoonotic disease with worldwide distribution caused by pathogenic Leptospira spp. Pathogenic Leptospira spp. are shed in urine of infected hosts and transmitted via ingestion of contaminated food or water, inoculation, inhalation of aerosolized urine, and absorption through mucous membranes. Leptospirosis is of particular concern in tropical and subtropical regions such as Barranquilla, Colombia. Recent reports indicate that in Barranquilla, rodents, dogs, and humans have a high leptospiral seroprevalence; and amongst zoo mammals, nonhuman primates have a high prevalence of Leptospira spp. infection. We therefore sought to determine whether primates in captivity at the Barranquilla Zoo were exposed to Leptospira spp. and whether there was a probable causal transmission link between the primates and peridomestic rodents. Samples were collected from 29 captive nonhuman primates, 15 free-ranging rats (Rattus rattus), and 10 freeranging squirrels (Sciurus granatensis). Serum samples from primates, rats, and squirrels were evaluated via microagglutination test (MAT) vs 24 reference Leptospira serovars. Blood and urine from the primates and kidney tissue from the rats and squirrels were cultured in Ellinghausen-McCullough-Johnson-Harris (EMJH) medium and polymerase chain reaction (PCR) of lipL32 was performed to determine whether active infection was present. Leptospiral seroprevalence was found to be 66.7% (10/15) in rats, 60% (6/10) in squirrels, and 6.9% (2/29) in neotropical primates. Ateles hybridus and Ateles fusciceps had positive titers to serogroups Cynopteri and Ictohaemorrhagiae, respectively. Of the rodents that had antibodies against Leptospira spp., 90% of the rats and 66.7% of the squirrels corresponded to the serovar australis. Interestingly, all animals were culture and PCR negative, indicating Leptospira spp. exposure in the absence of current infection. While their status as maintenance hosts needs to be investigated further, this is the first study to show leptospiral seropositivity in red-tailed squirrels (S. granatensis).

Intro

· Leptospirosis is the world’s most widely distributed zoonosis

· Leptospirosis is caused by pathogenic serovars of a bacterial spirochete of the genus Leptospira.

· Pathogenic Leptospira spp. are shed in urine of infected hosts

· Rodents have been recognized to be the most important and widely distributed reservoirs or maintenance hosts of leptospiral infection

· Leptospirosis is of particular concern in tropical/subtropical regions

· This paper sought to determine whether primates in captivity at the Barranquilla Zoo were exposed to Leptospira spp. and whether there was a probable causal transmission link between the primates and peridomestic rodents

M&M

· Samples were collected from 29 captive nonhuman primates, 15 free-ranging rats, and 10 free-ranging squirrels

· Serum samples from primates, rats, and squirrels were evaluated via microagglutination test (MAT) vs 24 reference Leptospira serovars.

· Blood and urine from the primates and kidney tissue from the rats and squirrels were cultured and PCR performed to determine whether active infection was present

Results and discussion

· Leptospiral seroprevalence was found to be 66.7% (10/15) in rats, 60% (6/10) in squirrels, and 6.9% (2/29) in neotropical primates

o The 2 NHP’s that were positive received untreated drinking water, other primates in the zoo received treated drinking water

· All animals were culture and PCR negative, indicating Leptospira spp. exposure in the absence of current infection

· Overall, 81.3% (13/16) of the rodents sampled (black rats and red-tailed squirrels combined), were seropositive against serovar australis. None of the captive nonhuman primates that were sampled were seropositive for serovar australis

· Given the distribution of Leptospira spp. serovars and the spectrum of maintenance reservoirs is very broad and heterogeneous, the results presented here need further evaluation to determine whether what is being observed is due to cross-reactivity and/or coinfection with less common serovars that may be circulating

· First study to show seropositivity in red tailed squirrels

Question 70

A recent study described pathology associated with spirurid infections in vervet monkeys.

What specific spirurid was this sutdy evaluating? What is its general life cycle? What are the intermediate hosts?

What were the most common lesions?

Answer 70

PATHOLOGY OF SPIRURID INFECTION IN VERVET MONKEYS (CHLOROCEBUS PYGERYTHRUS) HOUSED IN A PRIMATE REHABILITATION CENTER

Ana Navarro-Serra, DVM, PhD, Jaume-Vicent Jorda-Moret, DVM, PhD, and Hector Sanz-Cabanes, DVM, PhD

Abstract: Spirurids, specifically the Rictularia, Chitwoodspirura, Streptopharagus, and Protospirura genera, have been reported to parasitize all nonhuman primate taxa. Spirurid pathogenesis in nonhuman primates has not been reported frequently; however, Protospirura muricola has been associated with serious gastric pathologies, including gastric perforation. This study was a retrospective study of 38 vervet monkey (Chlorocebus pygerythrus) necropsies performed in a primate sanctuary that houses captive orphaned or injured wild-born vervet monkeys. Individuals were categorized according to their age, sex, and body condition score to investigate the relationships between these factors and parasite presence. This study identified P. muricola in 47.37% of the necropsied carcasses. Regarding individual factors associated with P. muricola infection, no significant differences between males and females were observed; however, relationships between parasite presence and poor body condition and advanced host age were observed. Furthermore, one monkey death was potentially directly related to spirurid pathogenic action, because the individual showed gastric perforation.

• Spirurid = parasitic nematode, in all nonhuman primate (NHP) taxa
• Protospirura muricola usually a rodent parasite, but common in NHPs
  
  • Adult worms in stomach or distal esophagus
  • Pathology dependent on worm burden but can → obstruction, perforation
  • Indirect life cycle - arthropods such as beetles, cockroaches, snails are intermediate hosts. L3 from intermediate infect definitive host
• This study evaluated relationship between infection, age, BCS, necropsy, histopathology
  
  • Retrospective - 38 necropsies from South African facility, died naturally
  • All infected animals had thickening of gastric wall - significant, especially where large numbers of adult worms were in the mucosa (e.g. pylorus)
    
    • Fibrosis of submucosa and visceral peritoneum. Some had nematodes in submucosa
  • No significant association between host sex and parasite load
  • Significant association between parasite presence and low BCS, geriatric age
    
    • Odds 38 times higher in geriatric animals, 33 times higher in low BCS
  • Protospirura muricola was only nematode detected, in 47% of animals necropsied
• Note that this facility had a higher prevalence of spirurids than in the field studies in central africa, but lower than wild vervets in South Africa. Captivity may change disease ecology

Take home: P. muricola is a pathogenic parasite in geratric captive vervet monkeys, also significantly associated with low body condition.

Question 71

A recent study described an outbreak of Lawsonia in nonhuman primates at a zoo.

What is lawsonia? What species does it typically affect? What are the typical lesions? What are the potential reservoir species?

What group of primates appear to be more susceptible?

Answer 71

Journal of Zoo and Wildlife Medicine 52(2): 680-688, 2021

PREVALENCE OF LAWSONIA INTRACELLULARIS INFECTION IN NONHUMAN PRIMATES AND PEST RODENTS IN A ZOOLOGICAL COLLECTION

Céline François-Brazier, DVM, Audrey Payebien, Christine Manson, DVM, Brice Lefaux, DVM, and Benoît Quintard, DVM, Dipl ECZM (ZHM)

Abstract: In 2016 and 2017, Lawsonia intracellularis was isolated from several pileated gibbons (Hylobates pileatus) presenting with diarrhea in Mulhouse Zoo (eastern France). To this day, infection with this bacterium has rarely been described in nonhuman primates (NHP) in captivity or in the wild and there are no data about the prevalence or transmission of the disease. This study focuses on finding the prevalence of this infection amongst Mulhouse Zoo’s NHP collection and trying to identify a source of contamination responsible for this epizooty. Forty-eight real-time PCR were conducted on feces from all NHP species in the zoo and on small mammals trapped in the NHP housing structures. No NHP was experiencing symptoms at the time of the study, however test results showed that Lawsonia intracellularis can be found in 61.76% (21/34) of the group total (n = 34) and the prevalence even increases to 92.3% (12/13) in the Lemuriform infraorder (n = 13). In small mammals (n = 14), prevalence of the bacterium is 57.17% (8/14) including 77.78% in rodents (7/9). The results of this study show that several NHP species are healthy carriers and some species of small mammals can be considered as a potential source of contamination. Because of the difficulty encountered trying to isolate the bacterium, it is plausible that infections caused by Lawsonia intracellularis have been underdiagnosed to this day, and that it could be an emerging disease in Europe. Therefore, using real-time PCR to search for this bacterium seems essential in case of diarrhea occurring in nonhuman primates. Moreover, even though further studies on contamination sources need to be conducted, the issue of the presence of rodents in NHP housing structures has to be taken very seriously and tackled with the utmost care.

Key Points:

• Lawsonia intracellularis
  
  • Curved gram-negative bacillus
  • Obligate intracellular enteropathogen
  • Causative agent for proliferative enteropathy primarily recognized in pigs (Sus scrofa domesticus), chickens (Gallus gallus), and horses (Equus caballus)
  • Replicates in the cytoplasm of intestinal epithelial crypt cells without killing them
  • Difficult to isolate
  • Reservoirs: rabbits (Oryctolagus cuniculus), Virginia possums (Didelphis virginiana), and coyotes (Canis latrans)
  • Transmission: direct contact between animals, feces of infected individuals, mechanical/biological vectors, interspecies transmission (mainly in immunosuppressed animals)
  • Can survive for up to 2 weeks under strict microaerophilic and thermal conditions
• Differences between and among infraorders were also noticed: Lemuriform > Simiiform
• Transmission through direct contact unlikely due to spatial distribution of the positive groups
• Indirect transmission via inanimate objects, keepers’ clothing, or contact unlikely due to strict biosecurity
• Suspect small mammals constituted direct or indirect animal vectors of L. intracellularis, allowing the bacterium. to be transmitted between NHP groups
  
  • No common shrew was infected à diet? (insectivorous vs. omnivorous mouse and field mouse)
• Outside of the epizooties in 2016 and 2017, no other NHP has presented with symptoms of L. intracellularis infection despite a group prevalence rate of almost 62%
  
  • Implies possible high rate of carrier animals
  • Only gibbons presented and died during the epizooties à immunosuppressed (Hep B) vs. sensitive?
  • PCR still strongly positive at 7 months after clinical recovery in the surviving gibbon from the 2017 epizooty à persistent carrier?

Take-Home Message:

• Several NHP species are healthy carriers
• Some species of small mammals can be considered as a potential source of contamination.
• Lawsonia infection should be included as a differential diagnosis of diarrhea in NHP and investigated via PCR on feces.
• Comprehensive rodent-control measures for enclosures where NHP are housed is paramount to reduce the probability of infection by Lawsonia intracellularis.
• Gibbons may be sensitive to L. intravellularis

Question 72

A recent study evaluated the morbidity and mortality of managed langurs in the UK.

What were the most common causes of death?

How commonly was hemosiderosis and Yersinosis reported?

Answer 72

Journal of Zoo and Wildlife Medicine 52(4): 1123–1134, 2021

A RETROSPECTIVE STUDY OF MORBIDITY AND MORTALITY IDENTIFIED AT POSTMORTEM EXAMINATION OF CAPTIVE LANGURS (TRACHYPITHECUS SPP) FROM SIX UNITED KINGDOM ZOOLOGICAL INSTITUTIONS: A 19-YEAR REVIEW

Marta Pereira, DVM, MSc, MRCVS, Mark F. Stidworthy, MA, VetMB, PhD, FRCPath, MRCVS, Daniela Denk, DECVP, MRCVS, DrMedVet, Simon Spiro, MVetMed, DPhil, DACVP, FRCPath, MRCVS, DECVP, Amanda Guthrie, DVM, DACZM, DECZM (ZHM), MRCVS, and Stuart Patterson, BVetMed, MSc, MVetSci, PhD, MRCVS

Abstract: Langurs are Asian primates belonging to the Colobinae subfamily. Langur populations are declining, with most species categorized as threatened by the International Union for Conservation of Nature. Investigation into the threats to population viability and sustainability would be beneficial but there is limited literature available on common diseases or causes of death in these species, either in captive or free-ranging settings. This study aimed to evaluate the most common causes of morbidity and mortality in Trachypithecus species submitted for postmortem examination by six United Kingdom zoological institutions between 2001 and 2020, to inform best practice husbandry guidelines. Necropsy and histopathology reports from 88 individuals of Trachypithecus species from six zoological organizations in the United Kingdom were analyzed. Species included Javan langurs (Trachypithecus auratus; n = 35), dusky langurs (Trachypithecus obscurus; n = 28), Francois langurs (Trachypithecus francoisi; n = 16), purple-faced langurs (Trachypithecus vetulus; n = 4), silvered langurs (Trachypithecus cristatus; n = 4), and Phayre’s langur (Trachypithecus phayrei; n = 1). Morbidities and causes of death were recorded. Gastrointestinal diseases and systemic infections were the leading causes of death (27.4% and 21.0% of cases where cause of death was known, respectively); linear foreign bodies were the most common cause of death. Interstitial pneumonia was frequently observed secondary to systemic infection. Heart abnormalities, anthracosis, and hemosiderosis were common but not directly associated with mortality. Further investigation is necessary to assess the importance of these conditions and whether they predispose to other diseases. This study provides a baseline for future research evaluating captive and free-ranging langur health and highlights husbandry practices that may decrease morbidity in these species.

Key Points:

• Langurs – primates form subfamily Colobinae
  
  • GI inflammation, bacterial infection, amoebiasis, foreign bodies, and trauma reported previously
• Objective: Assess most common morbidities and causes of mortality in langurs submitted from six zoos in the UK
• Mortality
  
  • Infectious disease was the most common etiology of cause of death
  • Silver langur in US – most common COD was trauma and nutrition-related
  • Intestinal plication and perforation due to linear foreign body (bark) were the most common cause of death
• Morbidity
  
  • Hemosiderosis most common morbidity reported, but no hemochromatosis
    
    • Most common disease to affect more than 1 organ system (liver, GI, spleen)
    • Diets in managed care are rich in iron and Vit C which enhances iron absorption
    • Hemosiderosis previously associated with Yersinia enterocolitica and Yersinia pseudotuberculosis
  • Heart disease – Cardiomyocyte AA, cardiomyopathy and myocardial fibrosis. Majority of CV disease not linked to cause of death.
    
    • Javan langur more predisposed than dusky langurs
  • GI disease:
    
    • Enteritis and colitis were most common GI diagnoses, often of infectious/inflammatory etiology.
    • Odds of enteritis higher in adult in geriatric animals; lower risk of enteritis in males
  • Systemic/Respiratory disease
    
    • Necrotizing hepatitis and splenitis occurred commonly and mostly caused by bacteria, presumed to be Yersinia pseudotuberculosis
    • Anthracosis and interstitial pneumonia most common morbidities in respiratory system
      
      • Anthracosis was most common respiratory abnormality but not associated with lung injury. Higher odds of having it if geriatric, but absence of higher odds in very geriatric (ger2) – potential exposure difference based on location
      • Associated with air pollution
    • Interstitial pneumonia – bacterial etiology in majority of cases, with most cases in animals suspected of septicemia, yersiniosis confirmed in most cases.
      
      • Dusky langur higher odds of than javan langur
      • Yersinia transmitted by rodents and wild birds
    • Pulmonary lesions mostly COD in neonate/hand reared (aspiration pneumonia/aspiration)

Take home: GI disease; systemic infections, namely Yptb infections; and linear foreign bodies represent an important source of morbidity and mortality in captive langurs.

References: None

Question 73

A recent study evaluated agreement of different blood analyzers for nonhuman primate samples.

How did the point of care analyzers compare to the reference laboratory values?

How did the analyzers compare to each other?

How did manual assessment compare?

Answer 73

Journal of Zoo and Wildlife Medicine 52(4): 1247-1256, 2021

COMPARISON OF THREE ANALYZERS FOR ASSESSING COMPLETE BLOOD COUNTS IN NONHUMAN PRIMATES

David E. Hannon and Matthew C. Allender – Reviewed by BCJ

Abstract: Diagnostic hematology can prove challenging to the exotic animal practitioner presented with a nonhuman primate patient. Few point-of-care automated cell counters are calibrated for primate samples. Twenty-one samples from 17 nonhuman primates presented to an exotic animal practice were analyzed. Samples were run on both canine and feline settings on each of two veterinary point-of-care analyzers: one that assays by impedance technology, and one that assays by laser flow cytometry. Samples were also sent to a reference laboratory to be assayed on an analyzer that performs simultaneous impedance and laser measurements of blood cells and has been calibrated for use in nonhuman primates. Fourteen analytes were assessed for each sample on each machine. Manual hematocrits and total white blood cell counts were also performed on 16 of the samples. Statistical analysis indicated some variance between individual parameters, but overall correlation was acceptable. 

Key Points:

• Agreement between all of the assays was good when evaluating granulocytes, neutrophils, lymphocytes, eosinophils, RBC, hemoglobin, and MCH.
• Agreement between the point-of-care analyzers and VRL was poorer when evaluating monocytes, hematocrit, mean corpuscular volume (MCV), MCHC, and platelets, but many of the values were still within the 95% CI and interquartile range of the reference laboratory
• Poor agreement with the samples that were assayed manually

Take-Home Message:

• Point-of-care impedance and laser flow cytometers calibrated for dog and cat samples can be used to obtain acceptable CBC results in NHP when these values are needed quickly.
• However, samples should ideally be submitted to a laboratory that uses equipment calibrated for NHP for the most accurate and precise results.

Question 74

A recent report described a case of fatal fascioloides in a lesser spot-nosed guenon.

Describe the general life cycle of Fascioloides magna. What is the intermediate and definitive hosts? How are abberrant hosts affected?

How did this guenon present?

What lesions were seen on necropsy?

Answer 74

Journal of Zoo and Wildlife Medicine, 52(4): 1309-1313, 2021

FATAL FASCIOLOIDES MAGNA IN A LESSER SPOT- NOSED GUENON (CERCOPITHECUS PETAURISTA)

Hasse, Kayla E., Garner, Michael M., Knightly, Felicia A., Sobotyk, Caroline, Luksovsky, Joe L., et al. – reviewed by ADW

Abstract: A 4-yr-old male intact lesser spot-nosed guenon (Cercopithecus petaurista), housed at a North American zoological facility, presented with acute lethargy, inappetence, and mild neurologic signs. Physical examination revealed hemorrhagic pleural effusion in the right hemithorax. This guenon’s condition improved over several days but then deteriorated, and the guenon presented with lethargy and weakness. A hemorrhagic pleural effusion was identified within the left hemithorax. The guenon developed respiratory and cardiac arrest while anesthetized. Gross examination revealed tract formation in the liver, adhesions of the liver to the diaphragm, hemorrhagic thoracic and abdominal effusion, and a single trematode within the right hemithorax. Morphologic features and species identification by PCR confirmed that the parasite was Fascioloides magna. Histologic examination revealed tract formation in the liver associated with biliary hyperplasia, fibrosis and hepatic necrosis, severe bile peritonitis, and pleuritis. This is the first report of an infection by F. magna in a primate.

Key Points:

• 4 yo MI lesser spot-nosed guenon w/ acute lethargy, weakness, hyporexia
  
  • PE: tachypnea (RR 60 brpm), hypothermia (96.8F)
  • CBC: mild anemia (HCT 30%)
  • CHEM: elevated hepatic enzymes (ALP 510, ALT 567)
  • RADS: marked pleural effusion in R hemithorax
  • THORACOCENTESIS: hemorrhagic effusion à 34% eosinophils, no infectious agents or neoplastic cells
  • Tx: bactracillin G, Excede, crystalloid fluids à improved over next few days
• 9 days later: acute lethargy, weakness, hyporexia
  
  • PE: tachypnea, low oxygen saturation (SpO2 83%)
  • CBC: progressive microcytic, hyperchromic anemia
  • CHEM: improved ALP 344 and ALT 85, elevated tBili 0.9, hypoproteinemia 5.2
  • Coagulation panel: prolonged PT, PTT, normal D-dimer
  • RADS: marked pleural effusion in L hemithorax
  • THORACOCENTESIS: 36 mL hemorrhagic fluid
  • Arrested during transport to facility for CT
• Gross Nx: pale white MM, pleural/abdominal hemorrhagic effusion, unclotted frank blood in bilateral hemithorax, 3 cm long trematode free-floating in R mid hemithorax, irregular black/green tracts in liver w/ blood-filled cavities, nodular quadrate lobe fractured at hilus, multiple adhesions btwn hepatic capsule & crux of diaphragm, tract communicating w/ thoracic cavity
• Histo:
  
  • Liver: severe biliary hyperplasia & fibrosis w/ hemorrhage, hepatocellular coagulative necrosis, marked cholestasis w/ bile lake microgranulomas; blood-filled tracts delineated by inflamed portal zones w/ hemosiderophages communicating w/ capsular surface associated with capsular fibrous adhesions
  • Diaphragm: moderate-severe peritoneal/pleural lymphoplasmacytic/histiocytic inflammation w/ adhesions and neovascularization
  • Pulmonary parenchyma: congested, edematous, variably atelectactic
  • SI, colon: moderately increased numbers of lymphocytes & plasma cells, increased crypts & glandular hyperplasia
  • Additional lesions attributable to trematodiasis or low-grade sepsis: myocarditis, pancreatitis, nodule in hippocampus
  • Trematode ID: Fascioloides magna – giant liver fluke of cervids
• Fascioloides magna – giant liver fluke of cervids
  
  • Indirect life cycle, infects snails as intermediate host, ungulates are definitive host
  • Infection in aberrant hosts often fatal d/t migration, lack of fluke encapsulation, associated severe hepatic damage
  • Diagnosis via fecal sedimentation
  • Anthelmintic treatment of dead-end hosts (sheep) often not effective due to low number of flukes required to kill dead-end hosts
• Unknown how this animal was infected à suspect ingestion of metacercaria in vegetation brought into enclosure

Take-Home Message: First case of F. magna in a primate highlights importance of consider aberrant parasitic migration and increasing biosecurity measures of food source or decreasing environmental snail abundance

Question 75

A recent global retrospective evaluated the pathological findings in Goeldi’s monkeys.

What is the scientific name of this species?

What is the most prevalent disease in this species?

What are risk factors for cardiac disease in this species?

Myelolipomas were commonly found where and in what demographic?

Yersinia infections are common where geographically?

Answer 75

GLOBAL RETROSPECTIVE ANALYSIS OF PATHOLOGICAL FINDINGS IN ZOO-MANAGED GOELDI’S MONKEYS (CALLIMICO GOELDII), 1965–2018
JZWM 2022 53(2) 339-348

Abstract: As part of the collaborative efforts and goals of managing zoo-housed Goeldi’s monkeys, or callimicos (Callimico goeldii), a retrospective review of gross and histopathological postmortem examination reports submitted to the International Studbook Coordinator was carried out by veterinary representatives of the Species Survival Plan to investigate disease trends. A total of 1,887 postmortem reports (1965–2018) collected from more than 150 institutions were reviewed. Histologic findings from 862 postmortem reports and primary causes of mortality were compiled to determine the most common findings. Within the study population, 419 individuals (48.6%) were male, 383 (44.4%) female, and the remaining 60 (7%) of undetermined sex. The primary lesion at death in adults was chronic renal disease. The other prevalent lesions included cardiac disease, myelolipomas, enteritis, colitis, and hepatitis. In Great Britain and mainland Europe, Yersinia spp. infection had significantly higher prevalence than in North American callimico populations. Multiple lesions affecting more than one organ system were identified in many animals of this study population. Results also showed that for adult callimicos in zoological institutions in North America, Europe, and Great Britain, life span has been increasing over the last 50 yr.

Intro
- The Goeldi’s monkey or callimico (Callimico goeldii) is a New World primate in the family Callitrichidae.
- The objectives of this study were to evaluate retrospectively the most common postmortem pathological findings from zoohoused callimicos over the last 54 yr and compare causes of morbidity and mortality in callimicos between sexes, age classes, decades, and location.

M&M
- 862 records with both histopathology and gross pathology, as well as known birth and death dates, were included in this study.
- These covered the period 1968 to 2018 and included 419 (48.6%) males, 383 (44.4%) females, and 60 (7%) animals of unknown sex.
- The animals sampled were from North America (n = 468, 54.29% of surveyed population), mainland Europe (n = 241, 27.96%), United Kingdom (n = 147, 17.05%), Asia (n = 1, 0.12%), and Africa (n = 5, 0.58%).
- From age at time of death distinct age classes were assigned on the basis of biological and clinical experience as follows: fetal (<24 h), neonate (24 h to 30 d), infant (31–364 d), young adult (1–4 yr), adult (5–8 yr), and geriatric (9 yr)

Results
- Renal disease was the most common diagnosis of most age classes, sexes, and continents
- Male callimicos >1 yr of age are significantly predisposed to developing renal disease, cardiac disease, and hepatitis, whereas females 1 yr of age are significantly predisposed to developing myelolipomas, neoplasia, dystocia, and metritis
- Callimicos 9 yr old have a significantly higher prevalence of renal disease (including nephritis and glomerulonephritis), myelolipomas, neoplasia, and cardiac disease, whereas callimicos 1–4 yr of age have a significantly higher prevalence of Yersinia spp. infection, trauma, and, for females, dystocia.
- In the 5–8 yr of age group, dystocia had the highest prevalence of all age classes in female callimicos. The prevalence of renal disease (including nephritis and glomerulonephritis), myelolipomas, neoplasia, and cardiac disease in callimicos between 5 and 8 yr was lower than the 9 yr of age group, but higher than the 1–4 yr of age group
- Differences were seen between most common lesions in North America and Europe
- Certain lesions also differed over decades (ie glomerulonephritis prevalence low in the 70s, high in the 90s)
- Yersinia spp. infection was 24.8 times more likely to be detected in Great Britain and 7.8 times more likely in mainland Europe than North America.
- Hepatitis was 1.51 times more likely to be reported in males
- Males on every continent were less likely than females to be observed with myelolipoma
- Parasitism and degenerative diseases were equally likely to be found in each demographic and location
- Males were less likely, and animals 9 yr were more likely to be observed with neoplasia.
- Cardiac disease was more likely in males, animals 5-8 yr and animals >9yr and less likely in animals from Europe than north america
- Age at death differed significantly over time (lifespan increasing over time)

Discussion
- Renal disease is the most prevalent and important disease in callimicos >1 yr of age.
– The cause of renal disease is unknown, but diet, vitamin D metabolism, immunoglobulin A through immunoglobulin M nephropathy and polyomavirus have been investigated with inconclusive results
- Cardiac disease also causes significant morbidity and mortality in callimicos
– Older males at higher risk
- Myelolipomas common, often found in the liver
– Risk factors for myelolipoma lesions were increasing age and sex; 45.2% of callimicos .9 yr and 31.2% of adult females had myelolipomas at postmortem exam
- Neoplasia was seen with increased frequency in female callimicos and aging animals
– Types of neoplasia too varied to characterize
- Yersinia spp. infection had higher incidence of pathology in callimicos from Great Britain (18.3%) and Europe (7%) than in North America (1%) for adults 1–8 yr of age.
- Prevalence of parasitic infections increased from 1980s to 2010s, possibly due to increase in natural substrate and/or better detection

Question 76

A recent study described rectal prolapse in the Sulawesie crested black macaque.

What is the scientific name of this species?

What diets have been links to rectal prolapse?

What social events were linked to rectal prolapse?

What pathogens were associated with prolapse?

How prevalent is rectal prolapse within this species?
- How is it commonly managed?
- What proportion of animals were euthanized for this condition?

Answer 76

RECTAL PROLAPSE IN THE SULAWESI CRESTED BLACK MACAQUE (MACACA NIGRA): MORBIDITY, MORTALITY, AND RISK FACTORS.
Van de Weyer Y, Rowden LJ, Guthrie A, Tahas SA.
Journal of Zoo and Wildlife Medicine. 2023;53(4):722-732.

Empirical data suggest that rectal prolapse (RP) is common in captive Sulawesi crested black macaques (Macaca nigra) in Europe, resulting in the euthanasia of animals that experience repeat occurrences. However, the prevalence, etiology, and risk factors of RP remain unidentified. The aims of this retrospective study were to assess the morbidity and mortality of RP, to provide an overview of management practices, and to identify risk factors for RP in this species. A questionnaire was sent to all European Ex situ Programme institutions that housed M. nigra between 01 January 2014 and 31 December 2020. Zoological Information Management System medical records and the studbook were used to obtain additional information. The questionnaire had a response rate of 65%, accounting for 204 animals. Of these animals, 25 (12.3%) suffered from at least one RP event during the study period and recurrence was noted in 72%. The majority of prolapses reverted naturally, but 28% of afflicted animals were euthanized for this ailment. Institutions with M. nigra with high frequencies of diarrhea (P= 0.035), those that provided diets of ≥90% vegetables and high-fiber pellet (P < 0.001), and those with more male than female M. nigra (P < 0.001) had increased odds of RP. Institutions that provided fruits daily (P < 0.002) had reduced odds of having RP cases. Although correlation of RP with diet was identified, confounding cannot be excluded, and a detailed dietary analysis needs to take place before altering feeding practices. Acute stressors and detection of protozoa in fecal samples were common findings before an RP event. Demographic analysis indicated that aged females, young males, and subordinate individuals were most affected by this condition. Where tested during an RP intervention, animals had low serum levels of vitamin D. Pedigree analysis hinted at genetic predisposition in this species and requires further investigation.

Background
- Sulawesi crested black macaque - critically endangered, poaching and habitat loss
– May be predisposed to severe, recurrent rectal prolapse

Key Points
- Frequent diarrhea, lack of daily fruit in diet, high veggie and high fiber pellets in diet, and more males than females increased likelihood of an institution experiencing cases of rectal prolapse
- Females experienced more prolapses than males especially adult/geriatric and multiparous
– Younger males frequently reported
- High % affected had a stressor within 1 mo of rectal prolapse
- Most had a subordinate social status
- Many had Balantidium coli or Entamoeba (associated with rectal prolapse in human children)
- Rectal prolapse reverted naturally in 80% and recurred in 72% cases
– 28% were euthanized, some at a young age
- Many had a first-degree relative that also had rectal prolapse (but confounding factor of high relatedness in zoo troops/populations

Conclusions
- Rectal prolapse is relatively common in Sulawesi crested black macaque
- Possibly associated with diarrhea, stressful events, subordinate status, higher male:female ratio, Balantidium coli and Entamoeba, geriatric age, older female with multiple offspring
– Vit D deficiency and genetics also a consideration
- Finding of decreased prolapse with daily fruit and increase prolapse with high fiber diet should be considered carefully as high fruit diets lead to a lot of other problems
- May not be recommended to breed females that have had a rectal prolapse due to possible heritability and negative effects of parturition on the pelvic floor

Question 77

A recent study described the longevity and juvenile mortality of zoo-housed mangabeys.

What is the scientific name of the grey-cheeked mangabey?
What is the scienfitic name of the black-crested mangabey?

Which species had higher juvenile mortality?
- How did the age of the mother affect survivorship of offspring?

Which sex had greater longevity?

Was a geographic association made with longevity?

Answer 77

Maximum longevity and juvenile mortality in zoo‐housed mangabeys.
de Visser M, Prins E, Bosse M, Crooijmans R, Ter Meulen T.
Zoo Biology. 2022;41(6):522-532.

Little is known about the biology of grey-cheeked and black crested mangabeys (Lophocebus albigena and Lophocebus aterrimus, respectively). As these primates face threats in the wild, well-monitored zoo-housed populations with up to date registries are becoming increasingly valuable to acquire species knowledge and to support conservation efforts. We used international studbooks to extract demographic and genetic information on 519 mangabeys to investigate how life history and parent-related variables influence maximum longevity and juvenile mortality. Generalized linear mixed models, as well as survival analyses, were applied. Results showed that females lived significantly longer than males, which is not uncommon in primates. Furthermore, our results indicated that the maximum longevity is lower for individuals living in European zoos versus individuals from North American zoos, which may be due to a combination of environmental differences and potential founder effects. We also show that the maternal maximum longevity is positively related to the maximum longevity of the offspring, which may be explained by the inheritance of “good genes“. However, the age of the mother at the moment of birth was negatively related to the maximum longevity of the offspring, which contradicts literature that states that, in primates, more experienced and thus older mothers will raise their offspring better than less experienced mothers. Instead, it is more likely that an “optimal age range” exists for breeding mothers. Our study provides insights into the population biology of captive mangabeys and may be helpful for identifying future research priorities to optimize primate health and welfare directly ex situ, and indirectly in situ.

Key Points
- Black crested and grey-cheeked mangabeys had no significant difference in maximum longevity
- Grey-cheeked had higher juvenile mortality (58%)
- Cumulative survival was generally higher in females than males
- No difference in maximum longevity of wild-born vs zoo-born mangabeys
- Maternal maximum longevity positively influenced offspring max longevity
- Age of mother at offspring birth negatively influenced maximum longevity of offspring (older mothers had young with shorter survival)
- No effect of rearing type of mother (parity) but juveniles more likely to survive longer if mother had fewer previous offspring
- No effect of paternal maximum longevity on offspring max longevity
- Adult mangabeys from North American zoos had overall higher cumulative survival than from European zoos
- Possible evidence of heritability of aging

Conclusions
- Zoo-housed black cresed and grey-cheeked mangabeys had longer survival in females, young with longer living mothers (likely heritable), and young with younger mothers at the time of birth
- With juvenile mortality cases, infants died sooner when the parity of the mother was lower but no effect of parity on maximum longevity of adults
- Adult mangabeys in NA zoos live slightly longer than EU zoos.