Clinical communication — Kliniese mededeling

Post mortem identification of Kalicephalus colubri colubri (Nematoda: Diaphanocephalidae) in a captive Mole (Pseudaspis cana) in South Africa

K Junkera, E P Laneb, B Dlaminib, A Kotzeb,c and J Boomkera*

containing colonies of tiny coccobacilli, ABSTRACT surrounded by layers of macrophages Necropsy examination of a captive emaciated, dehydrated adult female Mole snake and epithelioid cells. Bacterial culture of (Pseudaspis cana) in October 2007 revealed multiple cutaneous abscesses. Other findings these abscesses yielded a very mixed included renal and hepatic atrophy, hepatic haemosiderosis, multifocal granulomatous growth of bacteria, including a heavy hepatitis associated with acid-fast bacteria as well as pulmonary congestion and oedema. growth of Pseudomonas aeruginosa. Addi- Large numbers of the nematode Kalicephalus colubri colubri were recovered from the tional findings included atrophic kidneys oesophagus and stomach, representing the 1st reported case of K. colubri from a Mole snake with prominent urates and urate tophi, a in South Africa. The lesions caused by were insignificant, but the presence of K. c. colubri distended gall bladder, marked hepatic worms may have contributed to weight loss. atrophy, haemosiderosis and mild multi- Key words: cachexia, Kalicephalus colubri colubri, Nematoda, Pseudaspis cana, skin ulceration. focal granulomatous hepatitis with intra- Junker K, Lane E P, Dlamini B, Kotze A, Boomker J Post-mortem identification of lesional acid-fast bacteria, as well as Kalicephalus colubri colubri (Nematoda: Diaphanocephalidae) in a captive Mole snake moderately acute diffuse pulmonary con- (Pseudaspis cana) in South Africa. Journal of the South African Veterinary Association (2009) gestion and oedema. 80(1): 54–56 (En.). Department of Veterinary Tropical Diseases, University of Pretoria, Large numbers of filamentous red Private Bag X04, Onderstepoort, 0110 South Africa. helminths with a white head (<1.5 cm long) occurred in the empty oesophagus and stomach, many attached to the INTRODUCTION cephalus spp. in captive and free-ranging mucosa (Fig. 1), resulting in a moderately The Mole snake (Pseudaspis cana)isa in South Africa. Kalicephalus spp. diffuse heterophilic infiltration of the sub- constrictor with a wide distribution infection in snakes may be difficult to mucosa. While not all gastric nematodes throughout southern Africa. Its range diagnose as clinical signs such as lethargy were removed, a total of 73 specimens, extends northwards to Angola and and anorexia are non-specific. As with 57 females and 16 males, were collected eastwards to Kenya. In South Africa it other nematode infections, ante mortem and identified as Kalicephalus colubri colubri. inhabits a variety of habitats including diagnosis depends on identification of sandy scrubland in the southwestern adult parasites in regurgitated food or DISCUSSION Cape, Highveld grassland as well as faeces, by stomach endoscopy, or identifi- The cause of the Mole snake’s death was mountainous and desert regions. Living cation of nematode eggs in stomach considered to be a combination of meta- underground in abandoned burrows, its washings or faecal flotations9. Micro- bolic changes due to marked weight loss diet mainly consists of moles, scopic examination of oesophageal swabs and dehydration, as well as pulmonary and other small mammals, and therefore for eggs appears to give better results than oedema. Pulmonary oedema could have it is extremely useful in the control of cloacal swabs3. been caused by heart failure or hypopro- problem rodents. Although they are quite teinaemia due to severe weight loss and ferocious when captured and can inflict CASE HISTORY protein loss in the superficial cutaneous severe bites, Mole snakes soon settle In October 2007 a single adult female abscesses, as the tissues contained no down in captivity and are said to make Mole snake (186 cm long and weighing evidence of widespread systemic vascu- good pets2. 1.39 kg), which had been confiscated by lar damage associated with infectious This clinical communication illustrates the Gauteng Department of Agriculture, disease (septic shock)10. Marked weight some of the potential risks associated with Conservation and Environment 2 months loss, the distended gall bladder and organ maladaptation to captivity in recently previously, died while still in quarantine atrophy were indicative of long-term captured free-ranging snakes and intends at the Park at the National Zoolog- anorexia combined with high metabolic to draw the attention of exotic wildlife ical Gardens, Pretoria. A necropsy was need due to chronic infection. Possible practitioners to the occurrence of Kali- performed the same day. causes of anorexia in this snake include Necropsy revealed advanced autolysis, metabolic disease, parasitism, failure to aDepartment of Veterinary Tropical Diseases, University dehydration and severe fat and skeletal adapt to captivity and incorrect ambient of Pretoria, Private Bag X04, Onderstepoort, 0110 South Africa. muscle atrophy (cachexia). The snake had temperature. Anorexia and resultant bNational Zoological Gardens of South Africa, Pretoria, multiple skin ulcerations and foci of cachexia and dehydration may result PO Box 754, Pretoria, 0001 South Africa. depigmentation, <4 mm in diameter, from inappropriate environmental temper- cGenetics Department, University of the Free State, PO Box 339, Bloemfontein, 9300 South Africa mainly on the ventrum. Histologically ature and humidity as well as improper *Author for correspondence. these ulcers were associated with large feeding practices. Conversely, prolonged E-mail: [email protected] chronic subcutaneous abscesses consist- inactivity, inappropriate or unhygienic Received: June 2008. Accepted: February 2009. ing of fibrin and necrotic cellular debris substrate and/or inappropriate environ-

54 0038-2809 Tydskr.S.Afr.vet.Ver. (2009) 80(1): 54–56 especially Aeromonas and Pseudomonas, in at least 1 of the snakes, Kalicephalus was judged to be the causative organism. Clini- cal signs associated with Kalicephalus infection were lethargy and anorexia, especially in cases where the oesophageal lesions were severe3. On the other hand, some of the snakes infected with Kali- cephalus showed no hyperaemia or in- flammation, similar to the current case where few histological changes were associated with the parasite. Therefore, endoparasites might in themselves not necessarily be highly pathogenic, but the lesions caused by them can easily give rise to secondary bacterial infections13. Their demand on the host’s resources could make the latter more susceptible to serious pathogens, as the outcome of an individual’s reaction to an infectious agent is influenced amongst other factors by its energy resources1. Fig. 1: Kalicephalus colubri colubri attached to the gastric mucosa of Pseudaspis cana. Similarly, helminths are opportunistic parasites and a weakened immune system mental temperature ranges may have bica) and the Short-snouted grass snake on the part of the host often results in in- played a role in the development of the ( brevirostris brevirostris)7. creased intensities of infection. The com- cutaneous ulcers and abscesses5,11. Pseudo- Kalicephalus c. colubri has also been found paratively high intensity of Kalicephalus monas may have been a primary or sec- in P. cana in Kenya14, in Puff adders in the seen in the Mole snake is attributed to the ondary pathogen. It has been reported as Congo and in Zambia12,14 as well as in the debilitating effect of the multiple cutaneous one of the most common Gram-negative Forest cobra (N. melanoleuca) in West abscesses and the snake’s poor body con- bacterial organisms associated with lesions Africa14. This is the 1st report of K. c. colubri dition. in snakes11 and commonly colonises burn from a Mole snake in South Africa. In conclusion, the case presented here wounds such as those caused by lying on Despite the fact that not all the specimens highlights the need for parasitological heated pads8. Unfortunately, the hepatic present were collected, the intensity of screening of newly captive snakes, as well granulomas were microscopic and not K. c. colubri in P. cana was distinctly higher as those placed in quarantine. While seen at necropsy so liver tissue was not than that seen in free-ranging snakes in faecal examination is the most commonly submitted for further diagnostic evalua- South Africa, where the highest intensity used procedure for the non-invasive tion of the acid-fast bacterial infection. (40) was recorded from a Puff adder and detection of helminth infection, the Infections, usually with non-tuberculous the mean intensity of infection in the proposed higher efficiency of oesopha- mycobacteria, are seen sporadically in above-mentioned South African snakes geal swabs when compared with the well managed reptile collections. Clinical ranged from 1 to 10 (ref. 6). former3 would warrant investigation as disease, when it occurs, is generally Reports on the pathology caused by an additional diagnostic tool. chronic and progressive9. In this case, the Kalicephalus spp. are conflicting and the infection was mild, confined to the liver, parasites’ effect on the snakes seems to be ACKNOWLEDGEMENTS and probably of no clinical significance. strongly influenced by whether the hosts This communication arises from 4,9 Mycobacaterial infection in the snake are free-ranging or held in captivity . necropsy samples collected as part of a represents no zoonotic risk to human Kalicephalus inermis caused acute enteritis research project (07/17) at the National handlers or keepers, but mycobacteria are with mild lesions in recently caught Zoological Gardens: ‘Helminth parasites ubiquitous in soil, and humans, particu- free-ranging Pit vipers (Bothrops jacaraca) found during post mortem examinations larly immune-suppressed individuals, in South America, but caseous enteritis at the National Zoological Gardens of may become infected from the same associated with severe lesions in captive South Africa’. The first author is supported 4 source as the reptile. specimens that died at a serpentarium . by a University of Pretoria Post-doctoral The infection with K. c. colubri did not However, these vipers also had several Fellowship grant. cause significant inflammation in the other metazoan and protozoan parasites oesophagus and stomach, but may have in the respiratory and gastrointestinal REFERENCES affected appetite and subsequently tract which probably contributed to their 1. Bush A O, Fernandéz J C, Esch G W,Seed J R weight loss. Kalicephalus is one of the most deaths. Stress associated with captivity 2001 Parasitism: The diversity and ecology of common nematode genera parasitising may account for the fact that low parasite parasites (1st edn). University Press, 3,4,6 Cambridge: 20–21 snakes worldwide . In South Africa, K.c. burdens were severely debilitating to 2. Branch B 1998 Field guide to snakes and other colubri has been reported from 6 different captive snakes while only mild lesions of southern Africa (3rd edn). Struik, snake , the Puff adder (Bitis arie- were seen in heavily parasitised free- Cape Town tans), the Red-lipped herald (Crota- ranging snakes4. 3. Cooper J E 1971 Disease in East African phopeltis hotamboeia), the Brown house Kalicephalus spp. were found at necropsy snakes associated with Kalicephalus worms (Nematoda: Diaphanocephalidae). Veteri- snake (Lamprophis fuliginosus), the in 9 different snake species that died at 3 nary Record 89: 385–388 Snouted cobra (Naja annulifera), the the Nairobi Snake Park . While several of 4. Fernandes Grego K, Gardiner C H, Cato- Mozambique spitting cobra (Naja mossam- the snakes died of bacterial infections, Dias, J L 2004 Comparative pathology of

0038-2809 Jl S.Afr.vet.Ass. (2009) 80(1): 54–56 55 parasitic infections in free-ranging and Sauria (lizards). Onderstepoort Journal of Fowler M E, Miller R E (eds) Zoo & wild captive pit vipers (Bothrops jararaca). Veteri- Veterinary Research 67: 1–13 animal medicine (5th edn). W B Saunders nary Record 154: 559–562 8. Jacobsen E R 1981 Diseases of Reptiles. Part Company, London: 82–91 5. Frye F L 1986 Reptiles. In Fowler M E, Miller II. Infectious Diseases. Compendium on - 12. Peirce M A 1984 Some parasites of reptiles R E (eds) Zoo and wild animal medicine Continuing Education for the Practicing from Zambia and Indian Ocean islands (2nd edn). W B Saunders Company, Phila- Veterinarian 3: 195–200 with a description of Haemogregarina zam- delphia: 143 9. Jacobsen E R 2007 Parasites and parasitic biensis sp. n. from Dispholydus typus (Colu- 6. Hering-HagenbeckSFBN2001 The meta- diseases of reptiles. In Infectious diseases and bridae). Journal of Natural History 18: 211–217 zoan parasite fauna of South African rep- pathology of reptiles: color atlas and text. Taylor 13. Riley J 1986 The biology of pentastomids. tiles, with special attention to their nema- and Francis Group, LLC: 584–592 Advances in Parasitology 25: 45–128 todes. PhD thesis, Humboldt-University of 10. Kobzik L 1999 The lung. In Cotran R S, 14. SchadGA1962Studiesonthegenus Berlin Kumar V,Collins T (eds) Robbins pathological Kalicephalus (Nematoda: Diaphanocepha- 7. Hering-HagenbeckSFBN,Boomker J 2000 basis of disease (6th edn). W B Saunders lidae). II. A taxonomic revision of the genus A check list of the nematode parasites of Company, Philadelphia: 700 Kalicephalus Molin, 1860. Canadian Journal of South African Serpentes (snakes) and 11. Mitchell M 2003 Ophidia (Snakes). In Zoology 40: 1035–1167

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