4.2.1. Nutritional Requirements

Nutritional deficiencies, usually because of owner ignorance, are common problems in pet monkeys. The nutritional requirements of non-human primates are quite complex and vary greatly between the different species. Diets are complex and consist of fruits, vegetables, commercially available monkey chow, and food enrichment items. Primates may be primarily omnivorous, frugivorous, vegetarian, and foragers and their social standing may affect how much and what they eat.

Commercially available dietary products for both New World and Old World primates offer the most balanced nutrition. Vitamin supplementation is required if not using a commercially prepared food. This is critical for New World Primates who rely heavily on exogenous sources of vitamins C and D3. Foraging needs should be met in order to maintain mental enrichment standards.

Vitamin C deficiency is a common problem in NHP that are not properly supplemented. Although most commercial feeds have adequate levels of vitamin C at the time of packaging, after 90 days of storage, these levels decrease dramatically. Vitamin C deficiency typically presents as scurvy, with clinical signs including swelling of the epiphyses of long bones, hemorrhaging of the gums and periosteum and hydrocephalus. Maintenance levels of vitamin C are 1-4 mg/kg BW daily and treatment doses are up to 25 mg/kg twice daily for 5 days in severe cases.

Vitamin D3 deficiency: Both New World (esp. marmosets and tamarins) and Old World primates living in environments without sufficient sunlight require vitamin D3 supplementation. This should be present in commercial monkey diets. Avoid D2 or ergocalciferol since these cannot be utilized. Monkeys deficient in vitamin D3 develop soft bones (metabolic bone disease), long bone deformities, multiple fractures, and increased levels of serum alkaline phosphatase. Treatment consists of 2000 IU/kg vitamin D3 added to the diet. This treatment halts the progression of the process but the major bone deformities are irreversible. UVB or natural sunlight may be helpful in treatment and should be considered for prevention of the problem.

4.2.2. Hemochromatosis

Hepatic iron storage disease has been reported in lemurs. This is likely due to excessive dietary iron and the lack of tannins in the diet which are found in their natural environment (similar to the etiology suspected for toucans). Lemurs should be fed a special lemur commercial diet. Citrus fruits and/or added ascorbic acid should be avoided since this will increase the availability of iron. Hepatic neoplasia may be a consequence of hemochromoatosis.

5.1.1. Herpes Viruses

This viral family is one of the more common groups of viruses found in NHPs, as well as one of the best publicized. Herpes infections are responsible for a wide range of symptoms ranging from inapparent infections to fatal disease.

5.1.1.2. Other Pathogenic Herpes Viruses

Other herpes viruses that can be of concern, either because of zoonotic risks or transmission between susceptible species of monkeys are:

• Herpesvirus Hominis (Herpesvirus simplex): one of the oldest viral infections of man, two variants have been known to be transmissible from man to monkeys: HSV-1 and HSV-2 (experimentally). In owl monkeys, tree shrews, gibbons, marmosets and cebus monkeys, human herpesvirus causes high morbidity and mortality.
• Herpesvirus tamerinus : viral herpes in tamarins and marmosets that may cause severe clinical disease, including hepatitis, in those species. Can be devastating in owl monkeys. Appears to also be found in squirrel monkeys, cinnamon ringtails and spider monkeys often causing slight to no clinical disease.
• Epstein-Barr virus
• Spider Monkey herpesvirus : a herpes virus found in spider monkeys, and occasionally in capuchins, marmosets and wooly monkeys. Can be fatal in marmosets.
• Simian Varicellalike herpesviruses : This is a group of seven simian herpesviruses that closely resemble varicella-zoster in man. They include Liverpool vervet monkey virus, Patas monkey herpesvirus, Delta herpesvirus, Medical Lake macaque virus, Herpesvirus cyclopis, Chimpanzee herpesvirus, and Gorilla herpesvirus. Infection with any of the seven viruses, in general, causes high morbidity and mortality and varies greatly depending on the virus and species involved. Clinical signs can range from severe dermatitis to a severe, life threatening and often-fatal exanthematous disease.
• Simian Cytomegalovirus (CMV) : Cytomegalovirus is relatively host specific and in its natural hosts tends to cause latent infections with relatively no clinical signs.

5.1.2. Measles

Measles is an RNA paramyxovirus related to canine distemper and rinderpest. Although measles is not considered a naturally occurring disease in NHPs, it is one of the most frequently reported viral diseases. Infection in NHPs occurs as a result of human contact, and then the infected primate can shed the virus, and re-infect man. Clinical signs in NHP can range from fever, conjunctivitis, coryza, bronchitis and Koplik spots on oral mucosa. A skin rash may appear on the third to seventh day and leukopenia is common. Complications that may occur include otitis media, pneumonia, encephalitis, and enteritis. Measles infection in New World primates (marmosets, tamarins, and owl monkeys) is usually fatal and can be easily avoided by good husbandry practices and a vaccination program using an attenuated vaccine for both animals and staff.

5.1.3. Poxviruses

There are four types of poxviruses that infect NHP and three of these are zoonotic to humans. They can infect numerous species of NHP, usually presenting as typical cutaneous lesions, which can be severe enough to cause death. Monkeypox, caused by Monkeypox virus, is serologically related to smallpox virus in humans. The disease is characterized by proliferate dermal ulcerations and vesicles. Adult monkeys may get fevers but death is rare except in infants. Because Monkeypox is serologically related to smallpox, it has the potential to be devastating in unvaccinated human populations. Benign epidermal Monkeypox is a nonfebrile disease seen in macaques and is serologically related to Yaba tumor virus and is known as Yaba pox or Yaba like pox. The virus is identical to the agent that produces Tanapox in children in Africa. Yaba virus disease is seen in rhesus monkeys, baboons and rarely man. It appears as large subcutaneous, tumor like lesions.

5.1.4. Rabies

Nonhuman primates housed in rabies endemic areas are as susceptible to rabies as man. Only killed vaccines or vaccines suitable for use in humans should be used to vaccinate NHPs.

5.1.5. Polio

All NHP are extremely susceptible to polio, especially the great apes. In areas where polio vaccination of humans is routine, this usually does not present a problem to these animals due to the lack of disease in the human population. Because of their heightened sensitivity to polio, all monkeys, especially the great apes, should be vaccinated for the disease as juveniles.

5.1.6. Hepatitis

The viral infectious hepatitis virus (Hepatitis A) has been identified in chimpanzees, patas, wooley monkey, gorilla, cebus, aotus, and some tamarins. Antibodies to Hepatitis B (a lipid-enveloped DNA virus) have been reported in chimps and baboons, but the status of natural infection is not known. All great apes should be considered to be at risk for this infection (vaccination with the human product is available). Hepatitis B is one of the more commonly reported blood-borne pathogens isolated in the human health care setting. Most human cases that have been contracted from NHPs have resulted from contact with young or recently imported chimps. No fatalities have been reported as a result of a zoonotic transmission of hepatitis.

Hepataits C has been reported in chimpanzees and produces a chronic active hepatitis, cirrhosis and hepatocellular carcinoma.

5.1.7. Lymphocytic Choriomeningitis Virus (LCMV)

This rodent virus has been determined to be the cause of Callitrichid hepatitis. It presents as acute onset of lethargey anorexia and elevated liver enzymes. There is high mortality associated with this infection in captive collections. Monkeys are thought to get this infection from mice in the exhibit, or from being fed pinkie mice as treats in their diet. This practice should be avoided. This is a potential zoonotic concern.

5.1.8. Wasting Disease in Marmosets

The etiology of this syndrome has not yet been determined and may be the end result of several different diseases. Clinical signs usually involve weight loss and diarrhea. A lymphocryptovirus is one of the suspected etiologies, as well as gluten intolerance, vitamin E/selenium deficiency or stress induced. The pathologic lesion consists of enteric lymphoproliferation. Differential diagnosis should include bacterial enteritis (Salmonella, Campylobacter, E. Coli)

5.1.9. Other Zoonotic viruses

• Parainfluenza viruses
• Mumps
• Respiratory Syncytial Virus
• Rotavirus
• Poliovirus
• Coxsackievirus
• Rhinovirus

5.1.10. Filoviruses

Filoviruses belong to the family Filoviridae, one of several groups of viruses that can cause hemorrhagic fever in animals and humans. Marburg virus was the first filovirus to be discovered in 1967 in a shipment of African green monkeys imported into Marburg, Germany. There were 31 human cases associated with this outbreak and 7 of those were fatal. Then in 1976, Ebola virus was recognized in Zaire. Ebola virus has now been subtyped into these four distinct viral groups: Zaire, Sudan, Ivory Coast, and Ebola-Ralston. These relatively newly recognized strains of filoviruses have been given special attention due to the viral outbreak in a Virginia quarantine facility in recently imported cynomolgus monkeys (Ebola-Reston). No filovirus-related illness has been observed in any humans who have been in contact with these infected monkeys, but antibody titers have been detected, indicating transmission did occur. The three subtypes that are known to cause disease in humans are Ebola-Zaire, Ebola-Sudan and Ebola-Ivory Coast. The disease is called Ebola Virus Hemorrhagic Fever and clinical signs in both humans and NHP are: fever, chills, headaches, muscle aches, and anorexia. As the disease progresses, vomiting, diarrhea, abdominal pain, sore throat, and chest pain may develop. A coagulopathy then develops and bleeding may occur from injection sites as well as into the gastrointestinal tract, skin, and internal organs. Because of the high mortality rate from human filovirus infections (Ebola, Marburg-Europoe, Sudan and Zaire strains), the CDC has updated regulations and inspections of imported primates. Recent evidence has shown that wild primates, especially the great apes, may be susceptible to naturally occuring Ebola outbreaks in Africa. Current outbreaks are severely threatening key populations of lowland gorillas in central Africa (see CM Challenge).

5.1.11. Retroviruses

There are two groups of retroviruses that are endemic in human populations, the human T cell leukemia / lymphotropic viruses (HTLV) types I and II and the human immunodeficiency viruses (HIV) types 1 and 2. Non-human primates are the natural hosts for a variety of retroviruses including simian immunodeficiency virus (SIV), simian spumaviruses (simian foamy viruses (SFV), simian T-lymphotropic viruses (STLV), and/or simian type D retroviruses. All of these viruses cause life long infections in non-human primates and may be transmissible through sexual contact, blood, bodily fluids or breast milk. The risk of transmission of simian retroviruses to humans following occupational exposure to NHP is not totally understood, but is being studies. In 1993, the CDC and the National Institutes of Health implemented a voluntary testing and counseling surveillance program for SIV following detection of SIV in a worker at a primate facility. This study was later expanded to include voluntary testing and counseling for exposures to SFV, STLV, and simian type D retroviruses. There are significant implications for laboratory workers and zoo personnel that work with NHPs.

Simian Immunodeficiency Virus

• SIVs are lentiviruses, morphologically similar and biologically related to HIV-1 and HIV-2. SIV can cause acquired immunodeficiency syndrome (AIDS) - like illnesses in susceptible macaque monkeys and when it crosses from host-specific species to non-host specific species.
• SIV strains are not usually pathogenic in their natural host species.
• Presently monkeys with SIV are used extensively in the study of AIDS. SIV is genetically and antigenically related to HIV-2, resulting in substantial serological cross-reactivity. All of the simian viral isolates have characteristics in common with HIV, including some serological cross reactivity and suspected immune suppression resulting in clinical disease.
• Evidence of SIV infection has been reported for 30 different species of African nonhuman primates (see table 3). Two of these viruses, SIV_cpz from chimpanzees and SIV_sm from sooty mangabeys, have been shown to be the source of HIV1 and HIV2 and acquired immunodeficiency syndrome (AIDS) in humans. The relationship between simian retroviruses and the disease in humans is a great concern, especially with the recent increase in the Bushmeat Trade. Blood donation and organ donation research is also concerned with possible transmission of these viruses. There have been at least nine documented cases of humans infected with SIV (Hahn, et. al).

Table 3: African non-human primates infected with SIV

from Hahn, et al..

Foamy Viruses (Spumavirus genus of Retroviridae : SFV or Simian Spumaviruses)

• are more than 50% prevalent in captive NHP colonies of New and Old world origin.
• Spumaviruses differ from other retroviruses in several respects including the viral polymerase gene is expressed from a spliced sub-genomic RNA and the extracellular particle contains large amounts of reverse-transcribed DNA. Presently there are five antigenically distinct SFVs, three of which are: SFV-6 (chimpanzee), SFV-3 (African Green monkey), and SFV-2 (macaque).
• SFV can be readily isolated from infected animals saliva or from peripheral blood lymphocytes and it has been isolated in approximately 3% of tested laboratory and zoo workers with NHP exposure.
• To date, there have been no ill effects to health in either the humans that are positive for SFV or the positive NHP. This virus has been referred to as the virus in search of a disease, because it does have the capacity to incorporate itself into DNA and is routinely transmitted between NHP without signs of disease.

Simian Retrovirus 1

• (Type D retrovirus) has been documented to cause a form of chronic wasting immunodeficiency disease in several primate species, including the natural hosts.
• 0 - 90% of Asian macaques can be infected in a collection
• This disease has also been seen in Talapoins and Gelada baboons

Talapoin monkeys Miopithecus talapoin

Simian T-cell Lymphotropic Virus type 1

• STLV1 shares an extensive genomic sequence with human T-lymphotropic virus type 1 (HTLV1)and is associated with T-cell lymphomas in non-human primates.
• It is also pathogenic in natural hosts
• There is a 6.8% seroprevalence in susceptible captive populations

5.2.1. Mycobacterial Spp.

Mycobacteria are responsible for tuberculosis, an increasingly rare disease in captive primates. Old world species of primates appear to be more susceptible than New World species. Historically, the three major species of Mycobacteria - avium, bovis, and tuberculosis, have been incriminated as causing disease in NHPs. Recently, there have also been reports of atypical mycobacteria in NHPs. The primary route of transmission is through inhalation or ingestion.

Clinical disease can be hard to detect until the disease is in advanced stages. Clinical tuberculosis causes severe weight loss, lethargy, and coughing and is almost always fatal in NHP. In both humans and NHPs the skin test detects only TB exposure, not active disease. Active disease is diagnosed either by recovery of the organisms in culture or by thoracic radiographic lesions consistent with active TB. PCR and other amplification tests can also detect organisms. Treatment of positive, clinical NHP is not advised at this time due to both the fear of developing resistant strains of Mycobacteria as well as the risk to human handlers. All owners of NHP and others having contact with them, including veterinary staff, should be TB tested annually and if positive, also have thoracic radiographs annually under the guidance of a TB specialist.

5.2.2. Pseudotuberculosis

Yersinia pseudotuberculosis is a zoonotic, infectious bacterial agent that has a worldwide distribution and is endemic in European countries. The infection can affect a wide range of host species but in particular has caused numerous deaths in tamarins, marmosets and Goeldi's monkeys in captivity. Clinical signs of infection can range from asymptomatic animals that shed the bacteria, to nonspecific signs of systemic or enteric diseases or sudden death that may be difficult to diagnose. This disease can also produce a wasting syndrome. The organism can live in the soil for long periods of time and asymptomatic animals, combined with the difficulties in culturing the organism from rectal or fecal swabs, can all lead to difficulties in controlling the organism. Preventative measures such as quarantine, good sanitation, good hygiene, especially in food preparation, and pest control, together with a vaccination program in endemic areas, are all recommended in preventing infection, although vaccination is not 100% effective.

5.2.3. Bacterial Meningitis Syndrome

This syndrome seen in great apes has many etiologic agents and may be zoonotic depending on the agent involved. The syndrome can present as either acute or chronic meningitis and prompt, effective diagnosis and treatment is required to avoid fatalities or chronic, persistent clinical impairments. The most prevalent pathogens implicated are Streptococcus pneumoniae, Neisseria meningitides, and Hemophilus influenza type B.The N. meningitides and H. influenza type B are threats to exposed humans.

5.2.4. Campylobacter jejuni

Campylobacter jejuni is a common fecal bacterium found in old and new world monkeys. Asymptomatic shedding of large numbers of bacteria in feces is common. Some monkeys may exhibit mild to severe diarrhea accompanied by weight loss, dehydration and bloody feces. The disease in humans may cause debilitating diarrhea and people may also shed the bacteria asymptomatically.

5.2.5. Shigellosis

Shigellosis is common among old world monkeys. The most common species cultured in old world monkeys is Shigella flexneri, while the most common isolate from humans is S. sonnei. In most cases of zoonotic transmission humans are the reservoir for NHP infections. Shigella is very contagious to humans and children are very susceptible. Diarrhea with blood and mucus is the most common clinical sign in both humans and NHP. Shigella, if left untreated, may be rapidly fatal to NHP and human children.

5.2.6. Other Bacteria

Yersinia enterocolitica, Salmonella, and E. coli all can also be cultured from the GI tract of NHPs and are capable of causing zoonotic disease in humans. These organisms may or may not be associated with clinical disease in NHPs and one negative culture does not indicate a disease free animal.

5.3.1. GI parasites

Giardia lamblia, Cryptosporidium, Enterocytozoan bieneusi, Balantidium coli, and Entamoeba histolytica are all intestinal protozoa that can infect monkeys and humans. Diarrhea in both monkeys and humans can range from mild to severe. There have been a few documented cases of fatalities in neonatal and juvenile monkeys due to these protozoa.

There are also many nematode parasites seen in NHP. Some of the most frequently seen are Oesophagostomum, Strongyloides, and Dipetalonema species. Other GI parasites sometimes seen are Hymenolepis nana, Echinococcus granulosus and Prosthenorchus elegans. P. elegans is of particular importance in New World primates, especially tamarins and marmosets, and has been associated with high mortality in those species of monkeys. Preventative anthelmintics as well as diligent fecal screens and cockroach control are critical in maintaining these animals.

5.3.2. Blood borne parasites

Blood borne parasites are rare in captively bred monkeys but may be seen in wild caught monkeys. Trypanosoma cruzi has been isolated from recently imported squirrel monkeys, tamarins and marmosets and causes Chagas' disease. This is a disease that causes debilitation and cardiomyopathy in man.