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Case report: Control of intestinal nematodes in captive Chlorocebus sabaeus

There are limited data on the efficacy of antiparasitic treatments and husbandry methods to control nematode infections in captive populations of African green monkeys (AGMs), Chlorocebus sabaeus. In faecal egg count (FEC) tests, 10 of the 11 (91%) adult male AGMs captured from the large feral population on the island of St Kitts had evidence of nematode infections, mostly Capillaria (8/11, 73%), Trichuris trichiura (7/11, 64%) and strongylid species (7/11, 64%) specifically (hookworm and Trichostrongylus, 50/50), but also Strongyloides fuelleborni (1/11, 9%). When kept in individual cages with cleaning and feeding regimens to prevent reinfections and treated concurrently with ivermectin (300 µg/kg, given subcutaneously) and albendazole (10 mg/kg, given orally) daily for 3 days, 60% (6/10) of the AGMs were negative at a follow-up FEC at 3 months and by FEC and necropsy at the end of the study 5–8 months later. One monkey appeared to have been reinfected with T. trichiura after being negative by FEC at 3 months post-treatment. Four AGMs were positive for T. trichiura at the 3 month FEC follow-up but were negative at the end of the study after one further treatment regimen. Although initially being cleared of Capillaria following treatment, three AGMs were found to be infected at the end of the study. The ivermectin and albendazole treatment regimen coupled with good husbandry practices to prevent reinfections effectively controlled nematode infections in captive AGMs.


Introduction
Chlorocebus sabaeus, African green monkeys (AGMs) of the Cercopithecidae family, widely found in Africa, were introduced onto the Caribbean island of St Kitts in the 17th century (McGuire 1974). There are limited published data on the parasitic burden of the vast (perhaps 50 000; Dore, Gallagher & Mill 2021 -unpublished) feral population of AGMs, which commonly come into contact with people and may play a role in the epidemiology of human zoonotic parasitic infections common on the island (Berger 2020). Incomplete Caribbean studies have reported island AGMs to be infected with Trichuris trichiura (Yao et al. 2018), Strongyloides sp. (Gallagher et al. 2019;Ritchie et al. 1967), Primasubulura sp. (Cameron 1930) and Schistosoma mansoni (Cameron 1928).
There are limited data on effective anthelmintic treatments for AGMs and husbandry recommendations to control parasitic infections in captive research animals. Nonhuman primate research facilities require effective parasite treatment and prevention protocols to minimise infections that may confound research outcomes and cause unnecessary stress, which lowers the quality of life of study animals. Ritchie et al. (1967) reported that thiabendazole [two 50 mg/kg doses, PO 14 days apart] significantly reduced or eliminated Strongyloides eggs in the faeces. Kagira et al. (2011) reported that a 3-day regimen of albendazole (7 mg/kg, PO) and ivermectin (300 µm/kg, SQ) reduced the faecal egg counts (FEC) of T. trichiura and strongyles consistently by 100% after 7, 14 and 28 days. Chapman et al. (2016) reported that two doses of ivermectin (300 µg/kg, PO) 5 days apart resulted in a 100% cure rate for nematodes in wild AGMs, with no eggs found in the faeces 1 month posttreatment.
There are limited data on the efficacy of antiparasitic treatments and husbandry methods to control nematode infections in captive populations of African green monkeys (AGMs), Chlorocebus sabaeus. In faecal egg count (FEC) tests, 10 of the 11 (91%) adult male AGMs captured from the large feral population on the island of St Kitts had evidence of nematode infections, mostly Capillaria (8/11, 73%), Trichuris trichiura (7/11, 64%) and strongylid species (7/11, 64%) specifically (hookworm and Trichostrongylus, 50/50), but also Strongyloides fuelleborni (1/11, 9%). When kept in individual cages with cleaning and feeding regimens to prevent reinfections and treated concurrently with ivermectin (300 µg/kg, given subcutaneously) and albendazole (10 mg/kg, given orally) daily for 3 days, 60% (6/10) of the AGMs were negative at a follow-up FEC at 3 months and by FEC and necropsy at the end of the study 5-8 months later. One monkey appeared to have been reinfected with T. trichiura after being negative by FEC at 3 months post-treatment. Four AGMs were positive for T. trichiura at the 3 month FEC follow-up but were negative at the end of the study after one further treatment regimen. Although initially being cleared of Capillaria following treatment, three AGMs were found to be infected at the end of the study. The ivermectin and albendazole treatment regimen coupled with good husbandry practices to prevent reinfections effectively controlled nematode infections in captive AGMs. Unfortunately, the evaluation of nematode infections is challenging because of inadequate data on the drug efficacy in AGMs and the lack of studies investigating prolonged follow-up, which is needed to detect confounding factors (autoinfection, reinfection, larval transplacental or colostrum transmission, dormant stages and autoinfection resulting from parthenogenesis) (Reichard et al. 2017). Furthermore, FECs can be unreliable, and studies that enable necropsy evaluations are relevant in the absence of a 'gold standard' (Geary et al. 2010).

Keywords
In this report, we provide a more complete description of the nematode parasites present in AGMs on St Kitts and evaluate a treatment protocol and husbandry practices to control infections in captive AGMs.

Treatments
The deworming regimen was based on a report from Kenya (Kagira et al. 2011)

Monitoring of treatments
Day 0 and 3 month follow-up FECs were carried out on faeces collected directly from the cages. A final FEC and counts of adult T. trichiura in the large intestine were performed at routine necropsies 6 or 8 months after the initial IVAL treatment. For the recuperation of adult nematodes, the large intestine was carefully examined whilst removing the ingesta with a circular rubbing motion, washed with 0.9% saline, filtered through a 100-µm sieve and examined for nematodes under a stereomicroscope (7× -10× magnification).

Faecal analysis and morphologic identification
For FECs, aliquots (2 g) of uncontaminated faeces were collected from the cage's under-tray and analysed within 48 h using the double centrifugation technique (5 min, 500 g) with Sheather's sugar solution (spg 1.28). Eggs were identified to the species level whenever possible using described morphological characteristics (Modrý et al. 2015) ( Table 1 and Figure 1).
Infections, then, might have only been acquired in the 300 years since AGMs were introduced onto St Kitts. Unfortunately, we could not determine the Capillaria species involved as egg morphology alone cannot be used for speciation, and local experience is that no adults have been reported in the necropsy findings of AGMs on the island of St. Kitts.
Overall, the IVAL treatment regimen together with the husbandry measures in place in our study were relatively successful at controlling nematode infections in captive AGMs. Following a single IVAL treatment, 6/10 (60%) of the infected AGMs were negative for nematodes 6-8 months later as confirmed by FEC and at necropsy ( Table 2). A second IVAL treatment given to the four AGMs with persistent T. trichiura infections 3 months after the first treatment, resulted in the elimination of the T. trichiura 3-5 months later as evidenced by negative FECs and necropsy findings (Table 3). Although Note: Animals that tested negative by faecal egg count 3 months after treatment with ivermectin and albendazole were not re-treated whilst those that were positive were redosed with ivermectin and albendazole. FEC, faecal egg count; IVAL, ivermectin and albendazole; -, negative; + positive; T. trichiura, Trichuris trichiura; S. fuelleborni, Strongyloides fuelleborni.  apparently cleared of Capillaria following the first IVAL treatment, three of these four AGMs had Capillaria eggs in their faeces at necropsy 3-5 months after a second treatment.
The apparent treatment failures with T. trichiura and Capillaria described above warrant further comment. We suspect that the four AGMs that had T. trichiura eggs 3 months after the first treatment with IVAL most likely had infections in the prepatent period, which might exceed 12 weeks in humans (Bundy & Cooper 1989). It is also possible that the animals became infected whilst in captivity, which is the most likely explanation for the single AGM (Animal 7; Table 2) that was negative for T. trichiura 3 months after the first IVAL treatment but was positive for adults and eggs at necropsy after 8 months.
Trichuris eggs can remain inactive on surfaces for years (Bundy & Cooper 1989;Reichard et al. 2017), and although the AGM cages in our study were cleaned and disinfected regularly, Trichuris eggs are difficult to inactivate (Bundy & Cooper 1989). It is of note that six of these seven animals that were negative for FEC 3 months after the one IVAL treatment were still negative 6-8 months post-treatment. This indicates that the hygiene measures in use in our facility were mostly effective at preventing reinfection.
How four AGMs became positive for Capillaria following the apparent resolution of infection after the first IVAL treatment is unclear; without being able to determine the infecting specie/s, it is not possible to determine whether these AGMs had been in the prepatent period during treatment, were autoinfected, reinfected or had false-negative test results previously.
The main problem with the IVAL treatment regimen is the requirement for three consecutive sedations for albendazole administration; such repeated dosing, however, is needed for effective ovicidal and larvicidal activity (Martin, Robertson & Bjorn 1997). Further, this also enabled three administrations of ivermectin, which helps overcome the problem that single doses perhaps only temporarily inhibit the motion and feeding of nematodes instead of causing their death or expulsion (Martin et al. 1997).

Conclusion
African green monkeys can harbour several nematode species, and effective anthelmintic protocols are needed to ensure the optimal health and well-being of animals in captivity and to prevent zoonotic infections in handlers and local people. The IVAL treatment protocol and husbandry practices we describe would appear to be effective in controlling nematode infections in captive AGMs.