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. 1990 Oct;105(2):335–353. doi: 10.1017/s0950268800047932

Sex differentials in susceptibility to lymphatic filariasis and implications for maternal child immunity.

L Brabin 1
PMCID: PMC2271898  PMID: 2209738

Abstract

This paper reviews epidemiological data to see if there are sex differentials in prevalence, density and clinical pathology due to lymphatic filariasis. Of 53 studies from Africa, South East Asia, the Indian Subcontinent and The Americas, 43 showed a lower mean prevalence of infection in females than in males. Prevalence is consistently lower in women of reproductive age and this is statistically significant in 16 of 32 studies classified by age and sex. Density of infection is also lower in the reproductive age but may be higher in children and in older women. Clinical disease is also lower in women and pathology has a later age of onset and rise to peak prevalence than in males. The paper assesses the evidence that lower rates of infection and clinical pathology are due to less exposure of females to infective vectors. It seems unlikely that exposure alone could account for these differences which are observed for both bancroftian and brugian filariasis, irrespective of periodicity. Several investigators have suggested that females have increased resistance to infection and this is supported by serological studies showing high antibody positivity to adult worm antigens in females. The review concludes that the association with the reproductive years suggests a pregnancy-associated mechanism. This has important implications for maternal-fetal interactions and maternal filarial infection may influence the development of immunity in children.

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Selected References

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  1. ABDULCADER M. J., PADLEY R. Filariasis records in Ceylon. Indian J Malariol. 1960 Dec;14:521–543. [PubMed] [Google Scholar]
  2. Agarwal M., Prasad G. B., Harinath B. C., Bhatia B. D. Transplacental transfer of filarial infection. Indian Pediatr. 1986 Mar;23(3):169–174. [PubMed] [Google Scholar]
  3. Ash L. R. Preferential susceptibility of male jirds (Meriones unguiculatus) to infection with Brugia pahangi. J Parasitol. 1971 Aug;57(4):777–780. [PubMed] [Google Scholar]
  4. BASU P. C. Filariasis in Assam State. Indian J Malariol. 1957 Sep;11(3):293–308. [PubMed] [Google Scholar]
  5. BEYE H. K., KESSEL J. F., HEULS J., THOORIS G., BAMDRIDGE B. Nouvelles recherches sur l'importance, les manifestations cliniques, et la lutte contre la filariose à Tahiti, Océanie Francaise. Bull Soc Pathol Exot Filiales. 1953;46(1):144–163. [PubMed] [Google Scholar]
  6. Barclay R. Filariasis in Sabah, East Malaysia. Ann Trop Med Parasitol. 1969 Dec;63(4):473–488. doi: 10.1080/00034983.1969.11686650. [DOI] [PubMed] [Google Scholar]
  7. Barry C., Ahmed A., Khan A. Q. Endemic filariasis in Thakurgaon, East Pakistan. Am J Trop Med Hyg. 1971 Jul;20(4):592–597. doi: 10.4269/ajtmh.1971.20.592. [DOI] [PubMed] [Google Scholar]
  8. Bhattacharya N. C., Gubler D. J. A survey for bancroftian filariasis in the Calcutta area. Indian J Med Res. 1973 Jan;61(1):8–11. [PubMed] [Google Scholar]
  9. Brabin B. J. An analysis of malaria in pregnancy in Africa. Bull World Health Organ. 1983;61(6):1005–1016. [PMC free article] [PubMed] [Google Scholar]
  10. Bundy D. A. Gender-dependent patterns of infections and disease. Parasitol Today. 1988 Jul;4(7):186–189. doi: 10.1016/0169-4758(88)90076-2. [DOI] [PubMed] [Google Scholar]
  11. Chatterjee R. K., Singh D. P., Misra S. Dipetalonema viteae in Mastomys natalensis: effect of pregnancy and lactation on establishment and course of infection. Trop Med Parasitol. 1988 Mar;39(1):29–30. [PubMed] [Google Scholar]
  12. Chlebowsky H. O., Zielke E. Studies on Bancroftian filariasis in Liberia, West Africa. IV. Notes on side effects observed during a diethylcarbamazine treatment campaign in a rural area endemic for Wuchereria bancrofti and Onchocerca volvulus. Tropenmed Parasitol. 1980 Sep;31(3):339–344. [PubMed] [Google Scholar]
  13. Dennis D. T., Partono F., Atmosoedjono P. S., Saroso J. S. Timor filariasis: epidemiologic and clinical features in a defined community. Am J Trop Med Hyg. 1976 Nov;25(6):797–802. doi: 10.4269/ajtmh.1976.25.797. [DOI] [PubMed] [Google Scholar]
  14. Desowitz R. S., Hitchcock J. C. Hyperendemic bancroftian filariasis in the Kingdom of Tonga: the application of the membrane filter concentration technique to an age-stratified blood survey. Am J Trop Med Hyg. 1974 Sep;23(5):877–879. doi: 10.4269/ajtmh.1974.23.877. [DOI] [PubMed] [Google Scholar]
  15. Devereux D., Ash L. R. Increased susceptibility to infection with Brugia pahangi in aged female jirds (Meriones unguiculatus). J Parasitol. 1978 Feb;64(1):115–118. [PubMed] [Google Scholar]
  16. Dissanayake S., de Silva L. V., Ismail M. M. IgM antibody to filarial antigens in human cord blood: possibility of transplacental infection. Trans R Soc Trop Med Hyg. 1980;74(4):542–544. doi: 10.1016/0035-9203(80)90075-9. [DOI] [PubMed] [Google Scholar]
  17. Dutta S. N., Diesfeld H. J., Kirsten C. Der immunfluoreszenz-serologische Nachweis diaplazentar von Mutter auf Kind übertragener Serum-Antikörper gegen D. viteae als antigen in einem Wuchereria bancrofti-Endemiegebiet in Indien. Tropenmed Parasitol. 1976 Dec;27(4):479–482. [PubMed] [Google Scholar]
  18. Fan P. C., Wang Y. C., Liu J. C., Hsu J. Filariasis on Kinmen (Quemoy) Islands, Republic of China I. Parasitological investigation. Southeast Asian J Trop Med Public Health. 1974 Jun;5(2):211–222. [PubMed] [Google Scholar]
  19. Feinsod F. M., Faris R., Gad A., el Said S., Soliman B. A., Abd-el Azem I. S., Saah A. J. Clinical manifestations of Wuchereria bancrofti filariasis in an endemic village in the Nile Delta. Ann Soc Belg Med Trop. 1987 Sep;67(3):259–265. [PubMed] [Google Scholar]
  20. Grove D. I., Davis R. S. Serological diagnosis of bancroftian and malayan filariasis. Am J Trop Med Hyg. 1978 May;27(3):508–513. doi: 10.4269/ajtmh.1978.27.508. [DOI] [PubMed] [Google Scholar]
  21. Grove D. I., Valeza F. S., Cabrera B. D. Bancroftian filariasis in a Philippine village: clinical, parasitological, immunological, and social aspects. Bull World Health Organ. 1978;56(6):975–984. [PMC free article] [PubMed] [Google Scholar]
  22. Haque A., Capron A. Transplacental transfer of rodent microfilariae induces antigen-specific tolerance in rats. Nature. 1982 Sep 23;299(5881):361–363. doi: 10.1038/299361a0. [DOI] [PubMed] [Google Scholar]
  23. JORDAN P. Microfilarial density and infection rates of Wuchereria bancrofti and acanthocheilonema perstans in the Southern Province of Tanganyika Territory. Ann Trop Med Parasitol. 1955 Mar;49(1):42–53. doi: 10.1080/00034983.1955.11685650. [DOI] [PubMed] [Google Scholar]
  24. KANT L., PURI B. S., SEN S. K. Filariasis in Patna (Bihar). I. Indian J Malariol. 1956 Sep;10(3):199–217. [PubMed] [Google Scholar]
  25. KRISHNASWAMI A. K. Filariasis in Mangalore (South India). Indian J Malariol. 1955 Mar;9(1):1–16. [PubMed] [Google Scholar]
  26. KRISHNASWAMI A. K., RAGHAVAN N. G., SINGH J. Filariasis in Travancore-Cochin state. I. Ernakulam and Mattancherri. Indian J Malariol. 1956 Sep;10(3):219–238. [PubMed] [Google Scholar]
  27. Kazura J. W., Spark R., Forsyth K., Brown G., Heywood P., Peters P., Alpers M. Parasitologic and clinical features of bancroftian filariasis in a community in East Sepik Province, Papua New Guinea. Am J Trop Med Hyg. 1984 Nov;33(6):1119–1123. doi: 10.4269/ajtmh.1984.33.1119. [DOI] [PubMed] [Google Scholar]
  28. Klei T. R., Blanchard D. P., Coleman S. U. Development of Brugia pahangi infections and lymphatic lesions in male offspring of female jirds with homologous infections. Trans R Soc Trop Med Hyg. 1986;80(2):214–216. doi: 10.1016/0035-9203(86)90014-3. [DOI] [PubMed] [Google Scholar]
  29. Knight R., McAdam K. P., Matola Y. G., Kirkham V. Bancroftian filariasis and other parasitic infections in the Middle Fly River region of Western Papua New Guinea I. Clinical, parasitooogical and serological studies. Ann Trop Med Parasitol. 1979 Dec;73(6):563–576. doi: 10.1080/00034983.1979.11687298. [DOI] [PubMed] [Google Scholar]
  30. LIE KIAN JOE, HUDOJO, WIJONO, AMALIAH S. Wuchereria bancrofti infection in Djakarta, Indonesia. A study of some factors influencing its transmission. Indian J Malariol. 1960 Dec;14:339–352. [PubMed] [Google Scholar]
  31. MCCARTHY D. D., FITZGERALD N. I. Habit, habitat and hyperfilariation in the epidemiology of filariasis in Western Samoa. Trans R Soc Trop Med Hyg. 1956 Jan;50(1):58–65. doi: 10.1016/0035-9203(56)90009-8. [DOI] [PubMed] [Google Scholar]
  32. MCGREGOR I. A., HAWKING F., SMITH D. A. The control of filariasis with hetrazan; a field trial in a rural village (Keneba) in the Gambia. Br Med J. 1952 Oct 25;2(4790):908–911. doi: 10.1136/bmj.2.4790.908. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. MORISHITA K. An epidemiological aspects of filariasis in central Japan. Indian J Malariol. 1960 Dec;14:363–374. [PubMed] [Google Scholar]
  34. McFADZEAN J. A. Filariasis in Gambla and Casamance, West Africa. Trans R Soc Trop Med Hyg. 1954 May;48(3):267–273. doi: 10.1016/0035-9203(54)90075-9. [DOI] [PubMed] [Google Scholar]
  35. McGregor I. Current concepts concerning man's resistance to infection with malaria. Bull Soc Pathol Exot Filiales. 1983 Nov;76(5):433–445. [PubMed] [Google Scholar]
  36. McMahon J. E., Magayauka S. A., Kolstrup N., Mosha F. W., Bushrod F. M., Abaru D. E., Bryan J. H. Studies on the transmission and prevalence of Bancroftian filariasis in four coastal villages of Tanzania. Ann Trop Med Parasitol. 1981 Aug;75(4):415–431. doi: 10.1080/00034983.1981.11687461. [DOI] [PubMed] [Google Scholar]
  37. NAIR C. P. Filariasis in centrally administered areas. I. Filaria survey of Pondicherry Settlement. Indian J Malariol. 1960 Sep;14:233–252. [PubMed] [Google Scholar]
  38. NELSON G. S., HEISCH R. B., FURLONG M. Studies in filariasis in East Africa. II. Filarial infections in man, animals and mosquitoes on the Kenya Coast. Trans R Soc Trop Med Hyg. 1962 May;56:202–217. doi: 10.1016/0035-9203(62)90155-4. [DOI] [PubMed] [Google Scholar]
  39. Nathan M. B., Beckles G., Tikasingh E. S., Hamilton P. J., Monteil S. Parasitological and clinical studies of Wuchereria bancrofti and Mansonella ozzardi in coastal north Trinidad, West Indies. West Indian Med J. 1982 Dec;31(4):168–176. [PubMed] [Google Scholar]
  40. Oemijati S., Desowitz R. S., Partono F., Pant C. P., Mechfudin H., Sajidiman H. Studies on filariasis in the Pacific. 4. The application of the membrane filter concentration technique to a survey of Wuchereria bancrofti filariasis in Kepu district, Jakarta, Indonesia. Southeast Asian J Trop Med Public Health. 1975 Jun;6(2):186–189. [PubMed] [Google Scholar]
  41. Ottesen E. A., Mendell N. R., MacQueen J. M., Weller P. F., Amos D. B., Ward F. E. Familial predisposition to filarial infection--not linked to HLA-A or-B locus specificities. Acta Trop. 1981 Sep;38(3):205–216. [PubMed] [Google Scholar]
  42. Partona F., Djakaria, Oemijati S., Joesoef A., Clarke M. D., Cole W. C., Lien J. C., Cross J. H. Filariasis in West Kalimantan (Borneo), Indonesia. Southeast Asian J Trop Med Public Health. 1977 Dec;8(4):459–463. [PubMed] [Google Scholar]
  43. Partono F., Pribadi P. W., Soewarta A. Epidemiological and clinical features of Brugia timori in a newly established village. Karakuak, West Flores, Indonesia. Am J Trop Med Hyg. 1978 Sep;27(5):910–915. doi: 10.4269/ajtmh.1978.27.910. [DOI] [PubMed] [Google Scholar]
  44. Piessens W. F., McGreevy P. B., Ratiwayanto S., McGreevy M., Piessens P. W., Koiman I., Saroso J. S., Dennis D. T. Immune responses in human infections with Brugia malayi: correlation of cellular and humoral reactions to microfilarial antigens with clinical status. Am J Trop Med Hyg. 1980 Jul;29(4):563–570. doi: 10.4269/ajtmh.1980.29.563. [DOI] [PubMed] [Google Scholar]
  45. Piessens W. F., Wadee A. A., Kurniawan L. Regulation of immune responses in lymphatic filariasis. Ciba Found Symp. 1987;127:164–179. doi: 10.1002/9780470513446.ch11. [DOI] [PubMed] [Google Scholar]
  46. Raccurt C. P., Lowrie R. C., Jr, Katz S. P., Duverseau Y. T. Epidemiology of Wuchereria bancrofti in Leogane, Haiti. Trans R Soc Trop Med Hyg. 1988;82(5):721–725. doi: 10.1016/0035-9203(88)90214-3. [DOI] [PubMed] [Google Scholar]
  47. Raccurt C. P., Mojon M., Hodges W. H. Parasitological, serological, and clinical studies of Wuchereria bancrofti in Limbe, Haiti. Am J Trop Med Hyg. 1984 Nov;33(6):1124–1129. doi: 10.4269/ajtmh.1984.33.1124. [DOI] [PubMed] [Google Scholar]
  48. Rao C. K., Datta K. K., Sundaram R. M., Ramaprasad K., Rao J. S., Venkatanarayana M., Nath V. V., Rao P. K., Rao C. K., Das M. Epidemiological studies on bancroftian filariasis in East Godavari district (Andhra Pradesh): baseline filariometric indices. Indian J Med Res. 1980 May;71:712–720. [PubMed] [Google Scholar]
  49. Rao K. R., Venkatanaryana M., Naidu Y. D., Narasimham M. V., Viswanatham R., Rao C. K. Transplacental transmission in bancroftian filariasis. Indian J Med Res. 1984 Apr;79:495–496. [PubMed] [Google Scholar]
  50. Ripert C., Eono P., Eono D., Tribouley J., Appriou M., Issoufa H. Etude epidémiologique de la bancroftose dans la Vallee du Logone (Nord Cameroun). Med Trop (Mars) 1982 Jan-Feb;42(1):59–66. [PubMed] [Google Scholar]
  51. Sajidiman H., Desowitz R. S., Darwis F. Studies on filariasis in the Pacific. 5. Brugia malayi filariasis in treated and untreated populations of South Borneo. Southeast Asian J Trop Med Public Health. 1975 Jun;6(2):190–194. [PubMed] [Google Scholar]
  52. Schrater A. F., Spielman A., Piessens W. F. Predisposition to Brugia malayi microfilaremia in progeny of infected gerbils. Am J Trop Med Hyg. 1983 Nov;32(6):1306–1308. doi: 10.4269/ajtmh.1983.32.1306. [DOI] [PubMed] [Google Scholar]
  53. Udonsi J. K. Bancroftian filariasis in the Igwun Basin, Nigeria. An epidemiological, parasitological, and clinical study in relation to the transmission dynamics. Acta Trop. 1988 Jun;45(2):171–179. [PubMed] [Google Scholar]
  54. VARMA B. K., DASS N. L., SINHA V. P. Filariasis in the rural population around Bhagalpur Town. I. Indian J Malariol. 1961 Dec;15:285–292. [PubMed] [Google Scholar]
  55. VARMA B. K., DASS N. L., SINHA V. P. Filariasis in the rural population around Bhagalpur Town. II. Indian J Malariol. 1961 Dec;15:293–299. [PubMed] [Google Scholar]
  56. WILSON T. Filariasis in Malaya--a general review. Trans R Soc Trop Med Hyg. 1961 Mar;55:107–134. doi: 10.1016/0035-9203(61)90015-3. [DOI] [PubMed] [Google Scholar]
  57. Weil G. J., Hussain R., Kumaraswami V., Tripathy S. P., Phillips K. S., Ottesen E. A. Prenatal allergic sensitization to helminth antigens in offspring of parasite-infected mothers. J Clin Invest. 1983 May;71(5):1124–1129. doi: 10.1172/JCI110862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Weller P. F., Ottesen E. A., Heck L., Tere T., Neva F. A. Endemic filariasis on a Pacific island. I. Clinical, epidemiologic, and parasitologic aspects. Am J Trop Med Hyg. 1982 Sep;31(5):942–952. doi: 10.4269/ajtmh.1982.31.942. [DOI] [PubMed] [Google Scholar]
  59. Wijers D. J., Kinyanjui H. Bancroftian filariasis in Kenya II. Clinical and parasitological investigations in Mambrui, a small coastal town, and Jaribuni, a rural area more inland (Coast Province). Ann Trop Med Parasitol. 1977 Sep;71(3):333–345. [PubMed] [Google Scholar]
  60. Wilson T., Ramachandran C. P. Brugia infections in man and animals: long-term observations on microfilaraemia and estimates of the efficiency of transmission from mosquito vector to definitive host. Ann Trop Med Parasitol. 1971 Dec;65(4):525–546. doi: 10.1080/00034983.1971.11686786. [DOI] [PubMed] [Google Scholar]
  61. Wolfe M. S., Aslamkhan M. Bancroftian filiariasis in two villages in Dinajpur District, East Pakistan. I. Infections in man. Am J Trop Med Hyg. 1972 Jan;21(2):22–29. doi: 10.4269/ajtmh.1972.21.22. [DOI] [PubMed] [Google Scholar]
  62. Zielke E., Chlebowsky H. O. Studies on Bancroftian filariasis in Liberia, West Africa. I. Distribution and prevalence in the north-western savanna area. Tropenmed Parasitol. 1979 Mar;30(1):91–96. [PubMed] [Google Scholar]
  63. Zielke E., Chlebowsky H. O. Studies on bancroftian filariasis in Liberia, West Africa. II. Changes in microfilaraemia in a rural population some years after first examination. Tropenmed Parasitol. 1979 Jun;30(2):153–156. [PubMed] [Google Scholar]

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