Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-02T22:18:53.938Z Has data issue: false hasContentIssue false

Infectivity and virulence of Trypanosoma brucei metacyclics from Glossina morsitans morsitans salivary glands infected with tsetse DNA virus

Published online by Cambridge University Press:  19 September 2011

Walter G. Z. O. Jura*
Affiliation:
International Centre of Insect Physiology and Ecology (ICIPE), P.O. Box 30772, Nairobi, Kenya
Leonard H. Otieno
Affiliation:
International Centre of Insect Physiology and Ecology (ICIPE), P.O. Box 30772, Nairobi, Kenya
*
* Author to whom correspondence should be addressed.
Get access

Abstract

The pathogenicity of cyclically transmitted C16 clone 1 of Trypanosoma brucei metacyclics which developed within normal and hypertrophied DNA virus-infected salivary glands of Glossina morsitans morsitans was studied in the inbred, BALB/c mice. Microscopic examination of salivary glands obtained from G. m. morsitans with combined virus and T. brucei infections (i.e. the flies which transmitted the trypanosome infection to the test group of mice, group A) revealed that the glands comprised hyperplastic epithelial cells, some of which were fragmented, and numerous metacyclic trypanosomes. All the mice which contracted trypanosomiasis from G. m. morsitans with only T. brucei, i. e., the control mice (Group B; n=4) and the mice in the test group (n = 3) developed high parasitaemia and died. Repeated-measures analysis of variance using adjusted mean rate revealed that the mean prepatent periods and the mean times to death in both the control and the test groups of the BALB/c mice were not significantly different (P > 0.05). Analysis of log-transformed data fitted to a logistic growth model revealed that the rate of multiplication of T. brucei parasites in the blood of the test group BALB/c mice (r=2.373) was greater than in the control mice (r=0.808) and that the maximum carrying capacity was also attained earlier in the former group. These observations imply that the development of T. brucei metacyclics within hypertrophied salivary glands and their co-existence with the DNA virus particles might have enhanced their infectivity and virulence in the mice.

Résumé

La pathogénicité du clone 1 C16 (à transmission cyclique) des stades métacycliques de Trypanosoma brucei qui se sont developpés à l'intérieur des glandes salivaires normales et hypertrophiées infectées d'ADN viral de Glossina morsitans morsitans a été étudiée sur une lignée de souris, le BALB/c. L'examin microscopique des glandes salivaires obtenues sur G. m. morsitans porteuses d'infections mixtes virus et infections à T. brucei (cad les mouches ayant transmis l'infection à Trypanosoma au groupe test de souris, soit le group A) a révelé que les glandes abritaient des cellules épithéliales hyperplasiques dont certaines se présentaient en fragments et de nombreaux trypanosomes métacycliques. Toutes les souris ayant contracté la trypanosomiase à partir de G. m. morsitans avec les seuls T. brucei, cad les souris témoins (group B; n=4) et celles du groupe test (n=3) ont developpé une forte parasitémie et en sont mortes. L'analyse des mesures répétées de variance avec ajustement de moyennes a révelé que la période moyenne précédant la manifestation de la maladie et la période moyenne jusqu'au décès à la fois chez la groupe test et chez les témoins n'étaient pas significativement différentes (P > 0.05). L'analyse des données obtenues par transformation logarithmique et a justées à la courbe de croissance logistique a révelé que le taux de multiplication des parasites T. brucei dans le sang du groupe test BALB/c (r=2.373) était plus élevé que chez les souris témoins (r=0.808) et que la capacité maximum de charge était aussi atteinte plus tôt dans le premier groupe. Ces observations impliquent que le développement des T. brucei métacycliques à l'intérieur des glandes salivaires hypertrophiées et leur co-existence avec des particules virales d'ADN peuvent avoir modifié leur infectivité et leur virulence chez les souris.

Type
Research Articles
Copyright
Copyright © ICIPE 1994

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

Brenner, S. and Home, R. W. (1959) A negative staining method for high resolution electron microscopy of viruses. Biochem. Biophys. Acta 34, 103110.CrossRefGoogle ScholarPubMed
Burtt, E. (1945) Hypertrophied salivary glands in Glossina: Evidence that G. pallidipes with this abnormality is particularly suited to trypanosome infection. Ann. Trop. Med. Parasitol. 39, 1113.CrossRefGoogle Scholar
Burtt, E. (1946) Salivation by Glossina morsitans onto glass slides: A technique for isolating infected flies. Ann. Trop. Med. Parasitol. 90, 141144.CrossRefGoogle Scholar
Ellis, D. S. and Maudlin, I. (1987) Salivary gland hyperplasia in wild caught tsetse from Zimbabwe. Entomol. Exp. Appl. 45, 167173.CrossRefGoogle Scholar
Freund, R. J. and Littell, R. C. (1985) SAS Institute Inc. SAS for Linear Models. A Guide to the ANOVA and GLM Procedures. Cary, NC: SAS Institute Inc.Google Scholar
Gee, J. D. (1976) Active transport of sodium by Malpighian tubules of the tsetse fly, Glossina morsitans. J. Exp. Biol. 64, 357368.CrossRefGoogle Scholar
Herbert, W. J. and Parratt, D. (1979) Virulence of trypanosomes in the vertebrate host. In Biology of the Kinetoplastida (Edited by Lumsden, W. H. R. and Evans, D. A.), Vol. 2, pp. 481. Academic Press, London.Google Scholar
Hoare, C. A. (1972) The Trypanosomes of Mammals. Blackwell Scientific, Oxford.Google Scholar
Jaenson, T. G. T. (1978) Virus-like rods associated with salivary gland hyperplasia in tsetse, Glossina pallidipes. Trans. Roy. Soc. Trop. Med. Hyg. 67, 234238.CrossRefGoogle Scholar
Jura, W. G. Z. O. (1988) Morphological and functional changes associated with virus infection in male Glossina morsitans morsitans Westwood (Diptera: Glossinidae). In OAU/STRC, 1988, pp. 363372.Google Scholar
Jura, W. G. Z. O., Odhiambo, T. R., Otieno, L. H. and Tabu, N. O. (1988) Gonadal lesions in virus-infected male and female tsetse, Glossina pallidipes (Diptera: Glossinidae). J. Invertebr. Pathol. 52, 18.CrossRefGoogle ScholarPubMed
Jura, W. G. Z. O., Zdarek, J. and Otieno, L. H. (1993) A simple method for artificial infection of tsetse, Glossina morsitans morsitans larvae with the DNA virus of G. pallidipes. Insect Sci. Applic. 14(3), 383387.Google Scholar
Mihok, S., Otieno, L. H., Darji, N. and Munyinyi, D. (1992) Influence of D(+)-glucosamine on infection rates and parasite loads in tsetse flies (Glossina spp.) infected with Trypanosoma brucei. Acta Tropica 51, 217228.CrossRefGoogle ScholarPubMed
Otieno, L. H., Kokwaro, E. D., Chimtawi, M. and Onyango, P. (1980) Prevalence of enlarged salivary glands in wild populations of Glossina pallidipes in Kenya, with a note on the ultrastructure of the affected organ. J. Invertebr. Pathol. 36, 113118.CrossRefGoogle Scholar
SAS Institute (1987) SAS/STAT guide for personal computers, version 6 edition. SAS Institute Inc. Cary, NC, pp. 675712.Google Scholar
Sokal, R. R. and Rohlf, F. J. (1987) Biometry, 2nd ed. W. H. Freeman, San Francisco.Google Scholar
Southwood, T. R. E. (1987) Ecological Methods, 2nd ed. Chapman and Hall, London.Google Scholar
Van Meirvenne, N., Janssens, P. G. and Magnus, E. (1975) Antigenic variation in syringe passaged populations of Trypanosoma brucei. Ann. Soc. bélgé Med. Trop. 55, 123.Google Scholar