Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-19T02:12:43.720Z Has data issue: false hasContentIssue false
  • English
  • Français

Plasmodium chabaudi chabaudi chronic malaria and pathologies of the urogenital tract in male and female BALB/c mice

Published online by Cambridge University Press:  01 March 2004

M. BARTHÉLÉMY ,
P. N. VUONG ,
C. GABRION  and
G. PETIT
M. BARTHÉLÉMY
Affiliation:
Laboratoire de Parasitologie Evolutive CNRS UMR 7103, Cc 175, Université Pierre et Marie Curie, 9 quai Saint-Bernard, 75252 Paris Cedex 05, France
P. N. VUONG
Affiliation:
Unité d'Anatomie et de Cytologie Pathologiques, Hôpital Saint-Michel, 33 rue Olivier de Serres, 75015 Paris, France
C. GABRION
Affiliation:
Laboratoire de Parasitologie Evolutive CNRS UMR 7103, Cc 175, Université Pierre et Marie Curie, 9 quai Saint-Bernard, 75252 Paris Cedex 05, France
G. PETIT
Affiliation:
Laboratoire de Parasitologie Evolutive CNRS UMR 7103, Cc 175, Université Pierre et Marie Curie, 9 quai Saint-Bernard, 75252 Paris Cedex 05, France
Get access Rights & Permissions [Opens in a new window]

Abstract

BALB/c mice of both sexes were infected with a non-virulent strain of Plasmodium chabaudi chabaudi and any pathologies occurring in the urogenital tract and its accessory glands were investigated. Organs and tracts were removed from infected and control mice at 15, 40 and 100 days post-injection, weighed and processed for macroscopical and histological analyses. The relative weights of preputial, clitoral glands and testes were modified in infected mice during the 40 days following infection. The preputial glands show a marked hypotrophy at 15 days post-infection. The bladders of half of the infected female mice and a few infected male mice displayed a conspicuous haemoglobinuria and frequent interstitial cystitis that worsened throughout the experiment. Also, several chronic inflammatory reactions were detected in the prostates, preputial and clitoral glands up to 100 days post-infection. A probable cause of such a divergence in the characteristics of the infection and in the nature of the pathologies identified in infected male and female mice is the interaction between the infection and the immune and endocrine systems of the host. The cause of the pathologies and their consequences on the host condition are discussed.

Keywords

chronic malariaBALB/c miceurogenital tractpathologyhistologyPlasmodium chabaudi chabaudi
Type
Research Article
Information
Parasitology , Volume 128 , Issue 2 , February 2004 , pp. 113 - 122
Copyright
2004 Cambridge University Press

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

AKINGBADE, O., AINA, A. O., FOLASHADE, B. A. & MODUPE, M. J. (1990). Malaria parasitization and hormonal imbalance in virgin mice. Journal of the Medical Association of Thailand 73, 228–233.Google Scholar
ALEXANDER, J. & STIMSON, W. H. (1988). Sex hormones and the course of parasitic infection. Parasitology Today 4, 189–193.CrossRefGoogle Scholar
ANDRADE, H. F., CORBETT, C. E. P., LAURENT, M. D. & DUARTE, M. I. S. (1991). Comparative and sequential histopathology of Plasmodium chabaudi-infected BALB/c mice. Brazilian Journal of Medical and Biological Research 24, 1209–1218.Google Scholar
BARTHÉLÉMY, M., VUONG, P. N., GABRION, C. & PETIT, G. (2003). Oestrus cycle perturbations and hypotrophy of clitoral glands in malaria-infected female BALB/c mice. Parasitology Research 89, 134–140.CrossRefGoogle Scholar
BATSTONE, G. R., DOBLE, A. & GASTON, J. S. (2002). Autoimmune T cell responses to seminal plasma in chronic pelvic pain syndrome (CPPS). Clinical and Experimental Immunology 128, 302–307.CrossRefGoogle Scholar
BENTEN, W. P., WUNDERLICH, F., HERRMANN, R. & KUHN-VELTEN, W. N. (1993). Testosterone-induced compared with oestradiol-induced immunosuppression against Plasmodium chabaudi malaria. Journal of Endocrinology 139, 487–494.CrossRefGoogle Scholar
BENTEN, W. P., ULRICH, P., KUHN-VELTEN, W. N., VOHR, H. W. & WUNDERLICH, F. (1997). Testosterone-induced susceptibility to Plasmodium chabaudi malaria: persistence after withdrawal of testosterone. Journal of Endocrinology 153, 275–281.CrossRefGoogle Scholar
BRONSON, F. H. (1971). Rodent pheromones. Biology of Reproduction 4, 344–357.Google Scholar
BRONSON, F. H. & MARSDEN, H. M. (1973). The preputial gland as an indicator of social dominance in male mice. Behavioural Biology 9, 625–628.CrossRefGoogle Scholar
COX, F. E. G. (1988). Major animal models in malaria research: rodent. In Malaria: Principles and Practices of Malariology (ed. Wersdorfer, W. H. & Macgregor, I.), pp. 1503–1543. Churchill Livingston, Edinburgh, UK.
DE SOUZA, J. B. & RILEY, E. M. (2002). Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis. Microbes and Infection 4, 291–300.CrossRefGoogle Scholar
DELEON, D. D., ZELINSKI-WOOTEN, M. B. & BARKLEY, M. S. (1990). Hormonal basis of variation in oestrous cyclicity in selected strains of mice. Journal of Reproduction and Fertility 89, 117–126.CrossRefGoogle Scholar
EKVALL, H., ARESE, P., TURRINI, F., AYI, K., MANNU, F., PREMJI, Z. & BJORKMAN, A. (2001). Acute haemolysis in childhood falciparum malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 611–617.CrossRefGoogle Scholar
FELL, A. H. & SMITH, N. C. (1998). Immunity to asexual blood stages of Plasmodium: is resistance to acute malaria adaptative or innate? Parasitology Today 14, 364–368.Google Scholar
FERREIRA, A. L. & ROSSI, M. A. (1973). Pathology of the testis and epididymis in the late phase of experimental Chagas's disease. American Journal of Tropical Medicine and Hygiene 22, 699–704.CrossRefGoogle Scholar
GROOT, M. J. & DEN HARTOG, J. M. (1990). Histological changes in the genital tract of female veal calves implanted with naturally occurring anabolic steroids. Zentralblatt für Veterinärmedizin, A 37, 775–786.CrossRefGoogle Scholar
GROSSMAN, C. J. (1984). Regulation of the immune system by sex steroids. Endocrine Reviews 5, 435–455.CrossRefGoogle Scholar
GROSSMAN, C. J. (1989). Possible underlying mechanisms of sexual dimorphism in the immune response, fact and hypothesis. Journal of Steroid Biochemistry 34, 241–251.CrossRefGoogle Scholar
HAYASHI, S. & KIMURA, T. (1974). Sex-attractant emitted by female mice. Physiology and Behavior 13, 563–567.CrossRefGoogle Scholar
HUBLART, M., TETAERT, D., CROIX, D., BOUTIGNON, F., DEGAND, P. & BOERSMA, A. (1990). Gonadotropic dysfunction produced by Trypanosoma brucei brucei in the rat. Acta Tropica 47, 177–184.CrossRefGoogle Scholar
HUGGINS, C., PARSONS, F. M. & JENSEN, E. V. (1955). Promotion of growth of preputial glands by steroids and the pituitary growth hormone. Endocrinology 57, 25–32.CrossRefGoogle Scholar
KARLOVSKY, M. E. & PONTARI, M. A. (2002). Theories of prostatitis etiology. Current Urology Reports 3, 307–312.CrossRefGoogle Scholar
LAMANO CARVALHO, T. L., CARRARO, A. A., LOPES, R. A. & RIBEIRO, R. D. (1992). The male reproductive organs in experimental Chagas' disease. II. Morphometric study of the vas deferens in the chronic phase of the disease. Experimental and Toxicologic Pathology 44, 147–149.CrossRefGoogle Scholar
LANDAU, I. & GAUTRET, P. (1998). Animal models: rodents. In Malaria: Parasite Biology, Pathogenesis, and Protection (ed. Sherman, I. W.), pp. 401–417. ASM Press, Washington, D.C.
LANGHORNE, J., QUIN, S. J. & SANNI, L. A. (2002). Mouse models of blood-stage malaria infections: immune responses and cytokines involved in protection and pathology. Chemical Immunology 80, 204–228.CrossRefGoogle Scholar
LARRALDE, C., MORALES, J., TERRAZAS, I., GOVEZENSKY, T. & ROMANO, M. C. (1995). Sex hormone changes induced by the parasite lead to feminization of the male host in murine Taenia crassiceps cysticercosis. Journal of Steroid Biochemistry and Molecular Biology 52, 575–580.CrossRefGoogle Scholar
LEVESQUE, M. A., SULLIVAN, A. D. & MESHNICK, S. R. (1999). Splenic and hepatic hemozoin in mice after malaria parasite clearance. Journal of Parasitology 85, 570–573.CrossRefGoogle Scholar
LUCAS, P. D., DONOHOE, S. M. & THODY, A. J. (1982). The role of estrogen and progesterone in the control of preputial gland sex attractant odors in the female rat. Physiology and Behavior 28, 601–607.CrossRefGoogle Scholar
MALAGUARNERA, L. & MUSUMECI, S. (2002). The immune response to Plasmodium falciparum malaria. The Lancet Infectious Diseases 2, 472–478.CrossRefGoogle Scholar
MENENDEZ, C., FLEMING, A. F. & ALONSO, P. L. (2000). Malaria-related anaemia. Parasitology Today 16, 469–476.CrossRefGoogle Scholar
MESQUITA-GUIMARAES, J. & COIMBRA, A. (1981). The effect of sexual hormones on the lipid and proteinaceous secretion of the rat preputial sebaceous gland. Archives of Dermatological Research 270, 325–331.CrossRefGoogle Scholar
MITRA, S., DAGHER, A., KAGE, R., DAGHER, R. K. & LUBER-NAROD, J. (1999). Experimental autoimmune cystitis: further characterization and serum autoantibodies. Urological Research 27, 351–356.CrossRefGoogle Scholar
MORALES-MONTOR, J., GAMBOA-DOMINGUEZ, A., RODRIGUEZ-DORANTES, M. & CERBON, M. A. (1999). Tissue damage in the male murine reproductive system during experimental Taenia crassiceps cysticercosis. Journal of Parasitology 85, 887–890.CrossRefGoogle Scholar
OLSEN, N. J. & KOVACS, W. J. (1996). Gonadal steroids and immunity. Endocrine Reviews 17, 369–384.Google Scholar
OZEGOVIC, B. & MILKOVIC, S. (1972). Effects of adrenocorticotrophic hormone, growth hormone, prolactin, adrenalectomy and corticoids upon the weight, protein and nucleic acid content of the female rat preputial glands. Endocrinology 90, 903–908.CrossRefGoogle Scholar
RUDALI, G., ROUDIER, R. & VIVES, C. (1974). The preputial gland of the male mouse. Pathologie Biologie (Paris) 22, 895–899.Google Scholar
SCHALL, J. J. (1983). Lizard malaria: cost to the vertebrate host's reproductive success. Parasitology 87, 1–6.CrossRefGoogle Scholar
SCHALL, J. J. (1990). Virulence of lizard malaria: the evolutionary ecology of an ancient parasite–host association. Parasitology 100, S35–S52.CrossRefGoogle Scholar
SCHALL, J. J., BENNETT, A. F. & PUTNAM, R. W. (1982). Lizards infected with malaria: physiological and behavioral consequences. Science 217, 1057–1059.CrossRefGoogle Scholar
SCHALL, J. J. & DEARING, M. D. (1987). Malarial parasitism and male competition for mates in the western fence lizards, Sceloporus occidentalis. Oecologia 73, 389–392.CrossRefGoogle Scholar
STAHL, W., KANEDA, Y. & NOGUCHI, T. (1994). Reproductive failure in mice chronically infected with Toxoplasma gondii. Parasitology Research 80, 22–28.CrossRefGoogle Scholar
STAHL, W., KANEDA, Y., TANABE, M. & KUMAR, S. A. (1995). Uterine atrophy in chronic murine toxoplasmosis due to ovarian dysfunction. Parasitology Research 81, 109–113.CrossRefGoogle Scholar
TAVARES, M. C., CARRARO, A. A., FAVARETTO, A. L., PETENUSCI, S. O., LOPES, R. A., RIBEIRO, R. D. & CARVALHO, T. L. (1994). The male reproductive organs in experimental Chagas' disease. III. Plasma testosterone and accessory sex glands in the acute phase of the disease. Experimental and Toxicologic Pathology 46, 243–246.CrossRefGoogle Scholar
VAN DE MERWE, J. P. & ARENDSEN, H. J. (2000). Interstitial cystitis: a review of immunological aspects of the aetiology and pathogenesis, with a hypothesis. British Journal of Urology International 85, 995–999.CrossRefGoogle Scholar
VAN ZON, A., ELING, W. & JERUSALEM, C. (1978). Histo- and immunopathology of a malaria (Plasmodium berghei) infection in mice. Israel Journal of Medical Sciences 14, 659–672.CrossRefGoogle Scholar
VUONG, P. N., RICHARD, F., SNOUNOU, G., COQUELIN, F., RENIA, L., GONNET, F., CHABAUD, A. G. & LANDAU, I. (1999). Development of irreversible lesions in the brain, heart and kidney following acute and chronic murine malaria infection. Parasitology 119, 543–553.CrossRefGoogle Scholar
WUNDERLICH, F., MOSSMANN, H., HELWIG, M. & SCHILLINGER, G. (1988). Resistance to Plasmodium chabaudi in B10 mice: influence of the H-2 complex and testosterone. Infection and Immunity 56, 2400–2406.Google Scholar
ZHANG, Z., CHEN, L., SAITO, S., KANAGAWA, O. & SENDO, F. (2000). Possible modulation by male sex hormone of Th1/Th2 function in protection against Plasmodium chabaudi chabaudi AS infection in mice. Experimental Parasitology 96, 121–129.CrossRefGoogle Scholar