Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-05T05:08:41.477Z Has data issue: false hasContentIssue false
  • English
  • Français

Biology of Monanema globulosa, a rodent filaria with skin-dwelling microfilariae

Published online by Cambridge University Press:  05 June 2009

A. E. Bianco ,
R. Muller  and
G. S. Nelson
A. E. Bianco
Affiliation:
Dept. of Medical Helminthology, London School of Hygiene and Tropical Medicine, 395 Hatfield Road, St. Albans, Herts;
R. Muller
Affiliation:
Commonwealth Institute of Parasitology, St. Albans, Herts;
G. S. Nelson
Affiliation:
Dept. of Parasitology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, England
Get access Rights & Permissions [Opens in a new window]

Abstract

Monanema globulosa (Nematoda: Filarioidea) was recovered from four species of rodents in Kenya, with a prevalence of up to 94% in the striped mouse, Lemniscomys striatus. The adult worms are site-specific to the pulmonary arteries and release sheathed microfilariae that travel via the blood to the skin. Densities of microfilariea in the ears (mf/mg) were five to eight times greater than in any other region of the body and were directly proportional to the number of adult worms present. Highest concentrations of microfilariae in the skin were reached after 100 to 200 days and low numbers persisted in most animals for approximately 500 days.

Third-stage larvae from ticks (Haemaphysalis leachii) injected subcutaneously into jirds migrated widely through the body during early development. Moults occurred twice, after 5 to 10 days and 25 days, and the mean prepatent period was 75 (range 69 to 88) days. A mild eosinophilia developed which peaked after 29 days. Adults in the lungs provoked widespread and intense perivascular cuffing and more localized hypertrophy and fibrosis of the intima in arterioles. Dead adults caused granulomata which obliterated smaller vessels. Microfilariae in the skin elicited no local tissue reaction, but some which invaded the eyes caused a monocyte infiltration of the cornea. It is concluded that the parasite is well adapted to its natural hosts and that it has potential as a rodent model for human onchocerciasis because of the localization of microfilariae in the skin.

Type
Research Papers
Information
Journal of Helminthology , Volume 57 , Issue 3 , September 1983 , pp. 259 - 278
Copyright
Copyright © Cambridge University Press 1983

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, J., Fuglsang, H., Hamilton, P. J. S. & Marshall, T. F. de C. (1974) Studies on onchocerciasis in the United Cameroon Republic 1. Comparison of populations with and without onchocerciasis. Transactions of the Royal Society of Tropical Medicine and Hygiene, 68, 190–208.Google Scholar
Anderson, R. C. & Bain, O. (1976) Keys to genera of the Order Spirurida Part 3. Filarioidea, Aproctoidea and Diplotriaenoidea. CIH Keys to the Nematode Parasites of Vertebrates No. 3. (Anderson, R. C., Chabaud, A. G. and Willmott, S., Editors). Commonwealth Agricultural Bureaux, Farnham Royal, 59–116.Google Scholar
Anteson, R. K. (1968) Biological studies of Monanema marmotae (Webster, 1967) a filaroid parasite of the woodchuck Marmota monax canadensis. Unpublished Ph.D. thesis, University of Connecticut, 1968.Google Scholar
Aoki, Y., Recinos, M. M. & Hashiguchi, Y. (1980) Life span and distribution of Onchocerca volvulus microfilariae in mice. Journal of Parasitology, 66, 797–801.Google Scholar
Archer, R. K. (1963) The eosinophil leucocytes. Blackwell, Oxford.Google Scholar
Ash, L. R. (1971) Preferential susceptibility of male jirds (Meriones unguiculatus) to infection with Brugia pahangi. Journal of Parasitology, 57, 777–780.CrossRefGoogle ScholarPubMed
Beaver, P. C., Orihel, T. C. & Johnson, M. H. (1974) Dipetalonema viteae in the experimentally infected jird, Meriones unguiculatus II. Microfilaremia in relation to worm burden. Journal of Parasitology, 60, 310–315.Google Scholar
Bertram, D. S. (1947) The period required by Litomosoides carinii to reach the infective stage in Liponyssus bacoti, and the duration of the mites infectivity. Annals of Tropical Medicine and Parasitology, 41, 253–261.Google Scholar
Bertram, D. S. (1958) Some factors affecting microfilarial density and pathogencity in experimental epidemiology of an animal filarioid infection. Proceedings of the Sixth International Congress of Tropical Medicine and Malaria, 2, 437–443.Google Scholar
Bertram, D. S. (1966) Dynamics of parasitic equilibrium in cotton rat filariasis. In: Advances in Parasitology, 4, 255–319, Dawes, B. (Editor). Academic Press, London.Google Scholar
Beveridge, I., Kummerow, E. & Wilkinson, P. (1980) Experimental infection of laboratory rodents and calves with microfilariae of Onchocerca gibsoni. Tropenmedizin und Parasitologie, 31, 82–86.Google Scholar
Bianco, A. E. & Muller, R. L. (1977) A hard tick as vector of a new rodent filaria. Transactions of the Royal Society of Tropical Medicine and Hygiene, 71, 383.Google Scholar
Butterworth, A. E. (1980) Eosinophils and immunity to parasites. Transactions of the Royal Society of Tropical Medicine and Hygiene, 74, (Supplement), 38–43.Google Scholar
Chabaud, A. G. (1954) Sur le cycle évolutif des spirurides et de nématodes ayant une biologie comparable: valeur systématique des caractères biologiques. Annales de Parasitologie humaine et comparée, 29, 238–249.Google Scholar
Denham, D. A. (1974) Studies with Brugia pahangi 6. The susceptibility of male and female cats to infection. Journal of Parasitology, 60, 642.CrossRefGoogle ScholarPubMed
Denham, D. A., Dennis, D. T., Ponnudurai, T., Nelson, G. S. & Guy, F. (1971) Comparison of a counting chamber and thick smear methods of counting microfilariae. Transactions of the Royal Society of Tropical Medicine and Hygiene, 65, 521–526.Google Scholar
Denham, D. A., Ponnudurai, T., Nelson, G. S., Guy, F. & Rodgers, R. (1972) Studies with Brugia pahangi I Parasitological observations on primary infections of cats (Felis catus). International Journal for Parasitology, 2, 239–247.Google Scholar
Discombe, G. (1946) Criteria of eosinophilia. Lancet, 1, 195–196.CrossRefGoogle ScholarPubMed
Dissanaike, A. S. (1974) Two interesting blood parasites from wild rats in Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health, 5, 142–143.Google Scholar
Elbihari, S. & Ewert, A. (1973) Worm burdens and prepatent periods in jirds (Meriones unguiculatus) infected with Brugia malayi. Southeast Asian Journal of Tropical Medicine and Public Health, 4,184–186.Google Scholar
El Bihari, S. & Hussein, H. S. (1975) Location of the microfilariae of Onchocerca armillata. Journal of Parasitology, 61, 656.CrossRefGoogle ScholarPubMed
El Bihari, S., Hussein, H. S. & Muller, R. (1977) Monanema nilotica n.sp. (Nematoda: Onchocercidae) a cardiopulmonary parasite of the Nile rat in Sudan. Journal of Helminthology, 51, 317–321.Google Scholar
Fuglsang, H. & Anderson, J. (1974) Microfilariae of Onchocerca volvulus in blood and urine, before during and after treatment with diethylcarbamazine. Journal of Helminthology, 48, 93–97.Google Scholar
Fuglsang, H., Anderson, J. & Marshall, T. F. de C. (1976) The head nodule and ocular onchocerciasis in Africa. Tropenmedizin und Parasitologie, 27, 355–364.Google Scholar
Guyton, A. C. (1962) Textbook of medical physiology. W. B. Saunders Co., Philadelphia.Google Scholar
Johnson, M. H., Orihel, T. C. & Beaver, P. C. (1974) Dipetalonema viteae in the experimentally infected jird, Meriones unguiculatus 1. Insemination, development from egg to microfilaria, reinsemination and longevity of mated and unmated worms. Journal of Parasitology, 60, 302–309.CrossRefGoogle Scholar
Jordan, P. (1955) Observations on Wuchereria bancrofti and Acanthocheilonema perstans in Tanganyika. Transactions of the Royal Society of Tropical Medicine and Hygiene, 49, 460–471.Google Scholar
Kingdon, J. (1974) East African mammals. An atlas of evolution in Africa. Vol. II B. Academic Press, London.Google Scholar
Ko, R. C. (1972) The transmission of Ackertia marmnotae Webster, 1967 (Nematoda: Onchocercidae) of groundhogs (Marmota monax) by Ixodes cookei. Canadian Journal of Zoology, 50, 437–450.Google Scholar
Mackenzie, C. D. (1980) Eosinophil leucocytes in filarial infections. Transactions of the Royal Society of Tropical Medicine and Hygiene, 74, (Supplement), 51–58.CrossRefGoogle Scholar
Mellor, P. S. (1971) Studies on Onchocerca cervicalis (Railliet and Henry, 1910) and its development in Culicoides, Latreille. Unpublished Ph.D. thesis. University of London.Google Scholar
Muller, R. L. & Nelson, G. S. (1975) Ackertia globulosa sp.n. (Nematoda: Filarioidea) from rodents in Kenya. Journal of Parasitology, 61, 606–609.CrossRefGoogle ScholarPubMed
Murray, W. D. (1948) Filariasis studies in American Samoa. United States Naval Medical Bulletin, 48, 327–341.Google ScholarPubMed
Nelson, G. S. (1958) Onchoceriasis in the West Nile district of Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene, 52, 368–376.Google Scholar
Nelson, G. s. (1966) The pathology of filarial infections. Helminthological Abstracts, 35, 311–336.Google Scholar
Nelson, G. S. (1970) Onchocerciasis. In: Advances in Parasitology, 8, 173–224. Dawes, B. (Editor). Academic Press, London.Google Scholar
Nelson, G. S., Heisch, R. B. and Furlong, M. (1962) Studies in filariasis in East Africa II. Filarial infections in man, animals and mosquitoes on the Kenya coast. Transactions of the Royal Society of Tropical Medicine and Hygiene, 56, 202–217.Google Scholar
Nelson, G. S., Amin, M. A., Blackie, E. J. & Robson, N. (1966) The maintenance of Onchocerca gutturosa microfilariae in vitro and in vivo. Transactions of the Royal Society of Tropical Medicine and Hygiene, 60, 17.Google Scholar
Patnaik, B. (1962) Onchocerciasis due to 0. armillata in cattle in Orissa. Journal of Helminthology, 36, 313–326.CrossRefGoogle Scholar
Pratt, D. J., Greenway, P. J. & Gwynne, M. D. (1966) A classification of East African rangeland with an appendix on terminology. Journal of Applied Ecology, 3, 369–382.Google Scholar
Rabalais, F. C. (1974) Studies on Onchocerca cervicalis Railliet and Henry, 1910, microfilariae in the jird Meriones unguiculatus. Journal of Helminthology, 48, 125–128.Google Scholar
Rondell, P. A., Keitzer, W. F. & Bohr, D. (1955) Distribution of flow through capillaries and arterio-venous anastomosomes in the rabbit ear. American Journal of Physiology, 183, 523–525.Google Scholar
Scott, J. A., Macdonald, E. M. (1953) Experimental filarial infections in cotton rats. Experimental Parasitology, 2, 129–140.Google Scholar
Scott, J. A., Macdonald, E. M. & Terman, B. (1951) A description of the stages in the life-cycle of the filarial worm Litomosoides carinii. Journal of Parasitology, 37, 425–432.Google Scholar
Singh, M., Yap, E. H., Ho, B. C., Kang, K. L., Lim, E. P. C. & Lim, B. L. (1976) Studies on the Malayan forest rat filaris Breinlia booliati (Filarioidea: Onchocercidae): Course of development in rat host. Journal of Helminthology, 50, 103–110.Google Scholar
Solomon, G. B. (1969) Host hormones and parasitic infection. International Review of Tropical Medicine, 8, 101–158.Google Scholar
Spratt, D. M. & Varughese, G. (1975) A taxonomic revision of filarioid nematodes from Australian Marsupials. Australian Journal of Zoology, Supplement Ser. No. 35 (1975), 99 pp.Google Scholar
Townson, S., Bianco, A. E. (in press) Experimental infection of mice with the microfilariae of Onchocerca lienalis. Parasitology, 84.Google Scholar
Trevan, D. J. & Sharrock, A. (1951) A methyl green-pyronin-orange G Stain for formalin fixed tissue. Journal of Pathology and Bacteriology, 63, 326–329.Google Scholar
Wallenstein, W. L. & Tibola, B. J. (1960) Survey of canine filariasis in a Maryland area—incidence of Dirofilaria immitis and Dipetalonema. Journal of the American Veterinary Medical Association, 137,712–716.Google Scholar
Webster, W. A. (1967) Ackertia marmotae n.sp. (Filarioidea: Onchocercinae) from the groundhog (Marmota monax). Canadian Journal of Zoology, 45, 277–283.Google Scholar
Wenk, P. (1967) Der invasionweg der metazyklischen larven Litomosoides carinii Chandler 1931 (Filariidae). Zeitschrift für Parasitenkunde, 28, 240–263.Google Scholar
Wesley, I. V. (1973) Sex hormones and their influence on preferential susceptibility of the male jird (Meriones unguiculatus) to infection by Brugia pahangi (Nematoda: Filarioidea). Unpublished Ph.D. thesis, University of California.Google Scholar
Worms, M. J. (1970) Studies on the 1ife-history and biology of Onchocercidae (Leiper, 1911) (Nematoda: Filarioidea) with special reference to Dipetalonema setariosum (Mönnig, 1926) and Dipetalonema viteae (Krepkogorskya, 1933). Unpublished Ph D. thesis, University of London, 1970.Google Scholar
Zein-Eldin, E. A. (1965) Experimental infection of gerbils with Litomosoides carinii via intravenous injection. Texas Reports on Biology and Medicine, 23, 530–536.Google ScholarPubMed