Abstracts

BERTIELLOSIS IN MAN: A REVIEW OF CASES

Guillermo M. DENEGRI (1) & Jorge PEREZ-SERRANO (2)

SUMMARY

The presence of Bertiella mucronata and Bertiella studeri (Cestoda: Anoplocephalidae) in humans is reviewed, and international infection rates and a bibliography included. Taxonomic, biological, epidemiological, pathological, diagnostic, control, prevention and therapeutic aspects of the zoonosis are analyzed, and the increase in zoonotic potentiality of the parasitosis is discussed.

KEYWORDS: Bertiella mucronata; Bertiella studeri; Anoplocephalidae; Human cases; Review; Zoonotic potentiality.

INTRODUCTION

The genus Bertiella is very heterogeneous and includes cestodes parasitizing Marsupialia, Dermoptera, Rodentia and Primates in Africa, Asia, South America and Australia. Twenty-nine species were reported by SCHMIDT47 of which B. studeri and B. mucronata are known to infect man. In the Philippines, AFRICA & GARCIA3 found dogs infected by Bertiella. BLANCHARD8 described Bertia studeri from two non-human primates; Simia satyri and Troglodites niger. STILES & HASSAL49 revised the generic name of Bertia to Bertiella. MEYNER39 identified Taenia (Bertia) mucronata in a small monkey (Alouatta caraya = Mycetus niger) from Paraguay. The natural hosts in Africa and Asia for B. studeri are Simya satyrus, Anthropithecus troglodytes, Hylobates hoolock, Cercophithecus pygerythrus, C. schmidti, C. neglectus, C. sabaeas, C. mona mona, C. sabaensis, C. aethiops cynosusus, Cynomolgus sinicus, C. fascicularis, Troglodytes niger, Macaca cynomolgus, M. mulatta, M. rhesus, M. fascicularis, Pan spp., Papio ursinus and P. doghera. In South America the non-human primate hosts of B. mucronata are Alouatta carayá, Callicebus personatus nigrifrons, Cebus apella fatuellus, C. capuchinus and Callithrix sagui13,20,25.

DENEGRI20 analyzed the differences between human and monkey (A. caraya) B. mucronata isolates which he compared with B. studeri, elaborating on the geographic distribution of both species.

HUMAN CASES

BLANCHARD9 described the first human case in an 8 year old female from Mauritius Island parasitized by B. (satyri) studeri, confirming his previous suspicion8. CRAM17 found B. mucronata in three non human primates of the genus Pan, from three different regions of Africa, and in a human case from Spain. CRAM 17 noted that human infection may result from imported animals for exhibition or laboratory purposes (cited by STUNKARD 50). CRAM17 and CAMERON14 consider Bertiella as endemic to the West Indies, although the time and manner of its introduction are uncertain.

Table I summarizes the human cases reported to now due to B. studeri and B. mucronata with the corresponding geographical distribution. The data in Table I show the high prevalence of B. studeri in relation to B. mucronata. Up to the present moment, 44 cases of B.(=satyri) studeri, 7 cases of B. mucronata and 4 cases of inspecific Bertiella have been reported worldwide. The geographical distribution of B. studeri is the eastern hemisphere, a sole exception being those cases cited by CAMERON14 from St. Kitts Island (primates present on St. Kitts Island are known to be African, not American in origin) and STUNKARD et al.51 in a child in Minnesota, the latter considered to be the first autochthonous case in the United States of America. Recently, GALAN-PUCHADES et al.28 reported the first case of human bertiellosis in Spain. The geographical distribution of B.mucronata is South America, with three cases in Argentina, two in Brazil and one case each in Cuba and Paraguay26.

Records of human cases of Bertiella infection, age of infected individuals, and geographical distribution.

Geographical location Age
(Years) Species References Eastern hemisphere Mauritius 8 B. studeri Blanchard, 1913 9 India 2 B satyri Chandler, 1925 18 India ? B satyri Mukerji, 1927 40 India ? B satyri Sharma, 1930 48 India ? B satyri Sharma, 1930 48 India ? B satyri Sharma, 1930 48 India 8 B. studeri Maplestone, 1930 37 Sumatra ? B. studeri Joyeux & Dollfus, 1931 32 Mauritius 8 B. studeri Adams & Webb, 19332 Mauritius 4 B. studeri Adams & Webb, 1933 2 Mauritius 7 B. studeri Adams, 1935 1 Philippines 8 B. studeri Africa & Garcia, 1935 3 India 5 B. studeri Maplestone & Riddle, 1936 38 India 8 B. studeri Roy, 1938 45 Indonesia 7 B. studeri Bonne, 1940 11 East Africa 8 B. studeri Buckley & Fairley, 1950 12 Indonesia 4 B. studeri Lie Kian Joe, 1961 36 Indonesia 3,5 B. studeri Lie Kian Joe, 1961 36 Singapore 6 B. studeri Desowitz et al, 1961 24 Yemen ? B. studeri Fogh & Sertin, 1967 27 Great Britain 6 Bertiella sp. Thompson et al, 1967 53 Padang, West Sumatra 6.5 B. studeri Kwo & Koh, 1968 35 Medan, North Sumatra 7 B. studeri Kwo & Koh, 1968 35 Medan, North Sumatra 6 B. studeri Kwo & Koh, 1968 35 Selat Pandjang, Sumatra 14 B. studeri Kwo & Koh, 1968 35 Medan, North Sumatra 5 B. studeri Kwo & Koh, 1968 35 Medan, North Sumatra 6 B. studeri Kwo & Koh, 1968 35 Congo young Bertiella sp. Jones et al., 1971 31 Moscow, Russia 25 B. studeri Imamkuliev et al., 1983 30 India 29 Bertiella sp. Subbannayya et al., 1984 52 Thailand 26 B. studeri Bhaibulaya, 1985 7 Saudi Arabia 28 Bertiella sp. Bolbol, 1985 10 Gabon 2 B. studeri Richard-Lenoble et al, 1986 44 West Bengal, India 9 B. studeri Bandyopadhyay & Manna, 19876 Lampug, Indonesia 8 B. studeri Kosin & Kosin, 1992 34 Bangka, South Sumatra 5 B. studeri Kosin & Kosin, 1992 34 South Kalimantan, Indonesia 3,5 B. studeri Kosin & Kosin, 1992 34 Kalimantan, South Sumatra children B. studeri Kosin & Kosin, 1992 34 Palembang, South Sumatra children B. studeri Kosin & Kosin, 1992 34 Bengkulu, South Sumatra children B. studeri Kosin & Kosin, 1992 34 Bengkulu, South Sumatra children B. studeri Kosin & Kosin, 1992 34 Jambi, South Sumatra children B. studeri Kosin & Kosin, 1992 34 North Sumatra, Indonesia 3 B. studeri Kagei et al., 1992 33 North Sumatra, Indonesia adult male B. studeri Kagei et al., 1992 33 Orissa, India 4 B. studeri Panda & Panda, 1994 41 Valencia, Spain 33 B. studeri Galan-Puchades et al., 1995 28 Western hemisphere Cuba young B. mucronata Cram, 1928 17 St. Kitts Island young B. studeri Cameron, 1929 14 Brazil 29 B. mucronata Pessoa, 1930 42 Argentina 46 B. mucronata Bacigalupo, 1949 4 Paraguay 29 B. mucronata D' Alessandro et al., 1963 19 Minnesota, USA 5 B. studeri Stunkard et al., 196451 Brazil ? B. mucronata Costa et al., 1967 16 Argentina 45 B. mucronata Feldman et al., 1983 26 Argentina 2 B. mucronata Garaguso & Mendez, 1983, 29

In contrast to most cases of B. studeri infections reported in man have occurred in adults, not in children.

BIOLOGICAL CYCLE

Helminths belonging to the family Anoplocephalidae are heterotoxenic parasites that require and intermediate host to complete their life-cycle. The intermediate hosts are oribatid mites, important members of the soil fauna with a worldwide distribution. DENEGRI23 gives a list of oribatid mites which serve as the intermediate hosts of 14 genera and 27 species of anoplocephalid tapeworms.

With respect to the genus Bertiella, STUNKARD50 experimentally infected two species of oribatid mites; Scheloribates laevigatus and Galumna spp, with the eggs of B. studeri obtained from a non human primate (Macacus rhesus) from India. When the infected mites were fed on Macacus cynomolgus, no adult cestodes were obtained.

DENEGRI21,22 reported the experimental infection of two species of the family Oribatulidae, Dometorina suramericana and Scheloribates atahualpensis, with oncospheres of B. mucronata from man. D. suramericana showed a marked infection rate (18.1%) while in S. atahualpensis, the infection rate was only 0.6%, providing the definition of a potential biotope: "where components of the biological cycle of a parasite are not living together per se, but where, if introduced, each may survive to produce isolated phenomena (of parasitism) first, which thereafter generalizes if the "triggering"causes were to continue".

EPIDEMIOLOGY

Human infections due to Bertiella are usually accidental, in most cases, the patients have been in contact with monkeys either as pets or in the zoo. BAER5 in his paper "The origin of human tapeworms" refers to B.studeri, arguing that this parasite is mainly from sub-tropical climates although such climates are not fundamental for completion the life cycle. BAER suggests that Bertiella may be the only tapeworm to have been acquired by the prehominid ancestor of man and found in present day primates.

The opinion of BAER has been confirmed by FELDMAN et al.26 and GARAGUSO & MENDEZ29 who reported Bertiella in areas where the howler monkey (Alouatta caraya) is not present. DENEGRI21 demonstrated that B. mucronata cysticercoids undergo development in orbatid mites found in the living premises of a patient. This study determined the epidemiological chain of this parasitosis.

SANTA CRUZ et al.46 reported the parasitism of Alouatta carayá from the Argentinian Primate Center (CAPRIM, located in San Cayetano, Corrientes Province, Argentina). This work detected 29.4% infection (from a total of 74 A. caraya captured) by B. mucronata in agreement with DENEGRI20 . The latter noted that B. mucronata may be transmitted to human beings especially when parasitized monkeys arrive from the northern part of the country, due to specific circumstances (as in the case of FELDMAN el al.26, accidentally).

Thirty years before, in Bella Vista (Corrientes Province, Argentina) POPE43 found a 7% rate of infection (from a total of 84 howler monkeys examined) by B. mucronata.

DISEASE IN MAN

The infection in man apparently produces no overt symptoms although patients sometimes show episodes of abdominal pain, intermittent diarrhea, non-specific gastroenteritis, constipation, loss of appetite and weight, and general fatigue. In rare instances, the patient may complain of severe, recurrent abdominal pain with intermittent vomiting. Abdominal pain, loss of appetite and intermitent diarrhea often occur in children34. In one case, FELDMAN et al.26 described a patient that presented nervousness, hypertension, tachycardia, gastrointestinal indisposition and anal pruritus. All these symptoms disappear with appropriate therapy.

DIAGNOSIS

The diagnosis of Bertiella is based on (i) the identification of gravid proglottids and (ii) egg morphology. Gravid proglottids are several times wider than long, and are shed in groups of about 2 dozen at a time. The intermittent evacuations of worm segments in the feces caused the patients to seek medical treatment. Free eggs from the gravid segments or stool are 40-46 mm long and 36-40 mm wide in B. mucronata, and 49-60 mm long and 40-46 mm wide in B. studeri. The eggs of Bertiella have a characteristic pyriform apparatus measuring 22-24 mm in length by 16-18 mm in width in B. mucronata, and 25-30 mm in length by 18-28 mm in width in B. studeri20.

CONTROL AND PREVENTION

The control and prevention of this zoonosis are difficult since the intermediate hosts (oribatid mites) are cosmopolitan with a wide range of distribution21,23. DENEGRI20 has warned that the introduction of monkeys from where Bertiella is endemic and with which humans keep close contact, are the cause of parasite spreading. He also suggested an epidemiological inquiry in humans to ascertain the true prevalence of this parasitosis.

TREATMENT

Various antihelminthic agents are effective against Bertiella. Quinacrine34 given in a dosage for cestode treatment will promote evacuation of the whole tapeworm with the scolex. Other antihelminthics used for Bertiella are niclosamide (1-2g) given orally7,10,28,29,34,41 , praziquantel (10 mg/kg, single dose26,34) and albendazole34.

Praziquantel causes destruction of the parasite surface, producing lethal vacuolization26.

DISCUSSION

Since the first finding of Bertiella in man (19139), 55 cases have been registered. There has been a constant increase, in the number of cases, not only in tropical and subtropical regions, but at nearly all latitudes, suggesting the importance of the zoonosis for which biochemists, epidemiologists, physicians and sanitarians must be prepared.

A single characteristic, the presence of Anoplocephalid eggs eliminated in the feces, in addition to study of the bio-ecological conditions, allows the diagnosis.

Another alarming epidemiological fact is that first described by POPE43 , and later by COPPO et al.15 and SANTA CRUZ et al.46, that the parasitosis produced by B. mucronata in howler monkeys has increased 420% in only 30 years. An obvious question is: will human cases have increased at the same rate? Up to now the answer is negative. However, most described cases come from individual records given by physicians, and have not undergone proper epidemiological studies. We believe that the available data do not provide a true picture of the parasitosis in man and we suggest epidemiological inquiries to test this hypothesis.

RESUMEN

En este trabajo se hace una revisión de los casos humanos parasitados por Bertiella mucronata y Bertiella studeri (Cestoda: Anoplocephalidae), que incluye la casuística internacional y bibliografia actualizada. Se analizan varios aspectos de esta zoonosis como son: taxonomia, ciclo biológico, epidemiología, patologia, diagnóstico, control, prevención y terapéutica. Se discuten aspectos relacionados con la potencialidad zoonótica creciente de esta parasitosis.

ACKNOWLEDGEMENTS

The authors thank Dr. A. Criado and Dra. C. Sutton for reading this manuscript and providing linguistic assistance.

References

1. ADAMS, A. - A fourth case of human infestation with B. studeri (Cestoda) in Mauritius. Ann. trop. Med. Parasit., 29: 361-362, 1935.

2. ADAMS, A & WEBB, L. - Two further cases of human infestation with Bertiella studeri (Blanchard, 1891) Stiles & Hassall, 1902, with some observation on the probable synonymy of specimens previously recorded from man. Ann. trop. Med. Parasit., 27: 471-475, 1933.

3. AFRICA, C. & GARCIA, E. - The occurrence of Bertiella in man, monkey and dog in the Philippines. Philipp. J. Sci., 56: 1-11, 1935.

4. BACIGALUPO, J. - Primer caso humano de Bertiella sp. en Sud América. Rev. Soc. mex. Hist. nat., 10: 177-183, 1949.

5. BAER, J. - The origin of human tapeworm. J Parasit., 10: 127-134, 1940.

6. BANDYOPADHYAY, A & MANNA, B. - The pathogenic and zoonotic potentiality of Bertiella studeri. Ann. trop. Med. Parasit., 81: 465-466, 1987.

7. BHAIBULAYA, M. - Human infection with Bertiella studeri in Thailand. Southeast Asian J. trop. Med. publ. Hlth., 16: 505-507, 1985.

8. BLANCHARD, R. - Sur les helminthes des primates anthropoides. Mem. Soc. Zool. France, 4: 186-196, 1891.

9. BLANCHARD, R. - Bertiella satyri de l’Orang-outang, est aussi parasite de l’homme. Bull. Acad. Méd. (Paris)., 89: 186-296, 1913.

10. BOLBOL, A. - Bertiella sp. infection in man in Saudi Arabia. Ann. trop. Med. Parasit., 79: 643-644, 1985.

11. BONNE, C. - Over B studeri (Blanchard, 1891), B. satyri, (Stiles and Hassall, 1902), B. satyri (Blanchard, 1891). Geneesk. T. Ned.-Ind., 80: 2222-2230, 1940.

12. BUCKLEY, J. & FAIRLEY, N.- Demonstration of a cestode, Bertiella: a rare parasite in man and recorded for the first time as a human infection in Africa. Trans. roy. Soc. trop. Med. Hyg., 44: 2, 1950.

13. CABRERA, A. - Los monos de la Argentina. Physis, 16: 1-28, 1939.

14. CAMERON, T. - A new record of the occurrence of a tapeworm of the genus Bertiella in man. J. Helmint., 7: 231-234, 1929.

15. COPPO, J.; MORIENA, R. & LOMBARDERO, O. - El parasitismo de los primates del CAPRIM. Acta Zool. Lilloana, 35: 9-12, 1979.

16. COSTA, H.; CORREA, L. & BRENER, Z. - Novo caso humano de parasitismo por Bertiella mucronata (Meyner, 1895), Stiles & Hassall, 1902 (Cestoda-Anoplocephalidae). Rev. Inst. Med. trop. S. Paulo, 9: 95-97, 1967.

17. CRAM, E. - A species of the cestode genus Bertiella in man in chimpanzee in Cuba. Amer. J. trop. Med., 8: 339-345, 1928.

18. CHANDLER, A. - New records of B. satyri (Cestoda) in man apes. Parasitology, 17: 421-425, 1925,

19. D’ALESSANDRO, A.; BEAVER, P. & MAS PALLARES, R. - Bertiella infection in man in Paraguay. Amer. J. trop. Med. Hyg., 12: 193-198, 1963.

20. DENEGRI, G. - Consideraciones sobre sistemática y distribución geográfica del género Bertiella Stiles & Hassall, 1902 (Cestoda-Anoplocephalidae) en el hombre y en primates no humaos. Neotrópica., 31: 55-63, 1985.

21. DENEGRI, G. - Desarrollo experimental de Bertiella mucronata Meyner, 1895 (Cestoda-Anoplocephalidae) de origen humano en su huésped intermediario. Zbl. Vet.-Med., 32: 498-504, 1985.

22. DENEGRI, G. - Movilidad in vitro y poder infestante de oncósferas de Bertiella mucronata (Cestoda-Anoplocephalidae) de orígen humano. Rev. ibér. Parasit., 46: 59.61, 1986.

23. DENEGRI, G. - Review of oribatid mites as intermediate hosts of tapeworms of the Anoplocephalidae. Exp. appl. Acariol., 17: 567-580, 1993.

24. DESOWITZ, R.; WONG, H. & FERNANDO, M. - Thr first record of human infection with B. studeri in Malaya. J. Helminth., 35: 207-208, 1961.

25. DUNN, F. - Acanthocephalans and Cestodes of South American monkeys and marmosets. J. Parasit., 49: 717-722, 1963.

26. FELDMAN, R.; DENEGRI, G.; AVOLIO, J. & CANTU, N. - Nuevo caso humano de teniasis por Bertiella mucronata Meyner, 1895 (Cestoda-Anoplocephalidae) en la Argentina. I. Diagnóstico y tratamiento. Acta bioquim. clín. lat.-amer., 17: 571-578, 1983.

27. FOGH, S. & SERTIN, A. - Index-Catalog med. vet. Zool., 20: 1976.

28. GALAN-PUCHADES, M.; FUENTES, M. & MAS-COMA, S. - Parasitismo importado en Valencia: primer caso de Bertiellosis humana en España. In: Congreso Ibérico de Parasitología, 4., S. de Compostela, España, 1995. Resúmenes. p. 197-198.

29. GARAGUSO, P. & MENDEZ, O. - Primer caso argentino de parasitismo humano por Bertiella mucronata (Meyner, 1895). In: Congreso Latinoamericano de Parasitología, 6., S. Paulo, 1983. Resumos. p. 232.

30. IMAMKULIEV, K.D.; ALEKSEEVA, M.I.; GORBUNOVA, Y & BELIKOVA, G.G. - Bertielliasis: description of an imported case in USSR. Med. Parazit. (Mosk.), 4: 77-78, 1983.

31. JONES, R..; HUNTER, H. & VAN ROOYEN, C.E. - Bertiella infestation in a Nova Scotia child formerly resident in Africa. Canad. med. Ass. J., 104: 612, 1971.

32. JOYEUX, Ch. & DOLLFUS, R. - Un nouveau cas de B. studeri (R. Bl.) chez l’homme. C.R. Soc. Biol. (Paris), 107: 35-36, 1931.

33. KAGEI, N.L.; PURBA, Y. & SAKAMOTO, O. - Two cases of human infection with Bertiella studeri in North Sumatra, Indonesia. Jap. J. trop. Med. Hyg., 20: 166-168, 1992.

34. KOSIN, E. & KOSIN, L. Helminthic zoonosis in Indonesia. Yonsei Rep. trop. Med., 23: 81-88, 1992.

35. KWO, E. & KOH, I. - Six more cases of human infection with Bertiella studeri in Sumatra, Indonesia. Yonsey Rep. trop. Med., 23: 81-88, 1968.

36. LIE KIAN, J. - Inst. for Med. Res., Kuala Lumpur, Fed. of Malaya, 1961. Personal Communication to R.S. Desowitz.

37. MAPLESTONE, P. - A new case of B. studeri in a human. Indian med. Gaz., 65: 189-193, 1930.

38. MAPLESTONE, P. & RIDDLE, J. - Infection with B. studeri. Indian med. Gaz., 71: 81, 1936.

39. MEYNER, R. - Anatomie und histologie zweizr never Taenien artendes sub-genus Bertia. Z. Nat. Leips, 68: 1-106, 1895.

40. MUKERJI, A. - The incidence of helminthic infestations in the Carmichael Hospital for Tropical Diseases, Calcuta. Indian med. Gaz., 62: 695-696, 1927.

41. PANDA, D.N. & PANDA, M.R. - Report of Bertiella studeri (Blanchard, 1891), an anoplocephalid, from a child. Ann. trop. Med. Parasit., 88: 451-452, 1994.

42. PESSOA, S. - Sobre um caso de parasitismo humano por cestoide anoplocephalideo do genero Bertiella. Bol. Soc. Med. Cirurg., 14: 158-162, 1930.

43. POPE, B.L. - Some parasites of the howler monkey of northern Argentina. J. Parasit, 52: 166-168, 1966.

44. RICHARD-LENOBLE, D.; KOMBILA, M.; MAGANGA, M. & AFFRE, G. - Bertiella infection in a Gabon-born girl. Amer. J. trop. Med. Hyg., 35: 134, 1986.

45. ROY, S. - B. studeri, a natual tapeworm parasite of monkeys in a Hindu child. Indian med. Gaz., 73: 346, 1938.

46. SANTA CRUZ, A.; GOMEZ, L.; de ROTT, M. et al. - El parasitismo en Alouatta carayá y Saimiri boliviensis ingresados al "Centro Argentino de Primates". Rev. Med. vet. (B. Aires). 76: 150-152, 1995.

47. SCHMIDT, G.D. - CRC Handbook of tapeworm identification. Boca Raton, CRC Press, 1986.

48. SHARMA, A. - Helminthic infections in Shilong. Indian med. Gaz., 65: 200-203, 1930.

49. STILES, C. & HASSALL, A. - Bertiella new name for this cestodes genus Bertia Blanchard, 1891. Science, 16: 402, 1902.

50. STUNKARD, H. - The morphology and life history of the cestode Bertiella studeri. Amer. J. trop. Med., 20: 305-332, 1940.

51. STUNKARD, H.; KOIVASTIK, T. & HEALY, G. - Infection of child in Minnessota by Bertiella studeri (Cestoda-Anoplocephalidae) Amer. J. top. Med. Hyg., 13: 402-409, 1964.

52. SUBBANNAYYA, K.; ACHYUTHA ROA, K.; SHIVANANDA, P. et al - Bertiella infection in an adult male in Karnataka. A case-report. Indian J. Path. Microbiol., 27: 269-271, 1984.

53. THOMPSON, C.D.; JELLARD, C.H. & BUCKLEY, J.J. - Human infection with a tapeworm, Bertiella sp. probably of African origin. Brit. med. J., 254: 659, 1967.

Recebido para publicação em 11/01/1996

Aceito para publicação em 24/04/1997

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