Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-18T03:34:45.077Z Has data issue: false hasContentIssue false
  • English
  • Français

Glomerulonephropathies in Plasmodium inui-infected rhesus monkey: a primate model and possible applications for human quartan malaria

Published online by Cambridge University Press:  15 July 2014

L. F. NIMRI  and
H. N. LANNERS
L. F. NIMRI*
Affiliation:
Department of Medical Laboratory Sciences, Jordan University of Science and Technology, Irbid, Jordan
H. N. LANNERS
Affiliation:
Delta Regional Primate Research Center, Covington, LA 70433, USA
*
*Corresponding author: Department of Medical Laboratory, Jordan University of Science and Technology, Irbid, Jordan. E-mail: nimri@just.edu.jo
Get access Rights & Permissions [Opens in a new window]

Summary

None of the few animal models proposed for the study of human quartan malaria nephritic syndrome have shown complete pathological findings that are similar to those seen in humans. This study investigated the histopathological changes in kidneys in 10 Plasmodium inui infected Macaca mulatta monkeys by light and electron microscopy in order to develop a suitable animal model for human quartan malaria. Ten healthy adult rhesus monkeys were infected with P. inui and clinical chemistry and haematologic tests were done before and after infection. A renal biopsy sample was collected before infection as a baseline control and another biopsy was collected after infection. Histopathological changes examined by light and transmission electron microscopy (TEM) revealed abnormalities in all infected monkeys to variable degrees. Several electron-dense discrete or diffused mesangial deposits, and increase in mesangial cells and matrix were associated with the morphological changes observed by light microscope. This pattern is consistent with membranoproliferative glomerulonephritis type reported in humans infected with Plasmodium malariae. Results strongly support that the P. inui-infected rhesus monkey develop an immune-complex-mediated glomerulonephritis in the course of the infection. Therefore, this experimental model represents a useful tool to better understand the different parameters and the consequences of quartan malaria infections comparable to situations in humans.

Keywords

HistopathologyMacaca mulattaPlasmodium inuiquartan malariaglomerulonephritismicroscopy
Type
Research Article
Information
Parasitology , Volume 141 , Issue 12 , October 2014 , pp. 1638 - 1645
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

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

Abdurrahman, M. B., Greenwood, B. M., Narayana, P., Papaoye, F. A. and Edington, G. M. (1981). Immunological aspects of nephritic syndrome in Northern Nigeria. Archives of Disease in Childhood 56, 199–202.Google Scholar
Adedoyin, O. T., Gbelee, H. O. D. and Adeniyi, A. (2001). Childhood nephrotic syndrome in Ilorin. Nigerian Journal of Paediatrics 28, 68–72.Google Scholar
Adeniyi, A., Hendrickse, R. G. and Houba, V. (1970). Selectivity of proteinuria and response to prednisolone or immunosuppressive drugs in children with malaria nephrosis. Lancet 1, 644–648.CrossRefGoogle ScholarPubMed
Aikawa, M., Broderson, J. R., Igarashi, I., Jacobs, G., Pappaioanou, M., Collins, W. E. and Campbell, C. C. (1988). An Atlas of Renal Disease in Aotus Monkeys with Experimental Plasmodial Infection, pp. 1–97. American Institute of Biological Sciences, Washington, DC.Google Scholar
Barnwell, J. and the Plasmodium Comparative Genomics Writing Group (2007). Neglected burden of human vivax malaria: comparative analysis of Plasmodium vivax and key related species. www.genome.gov/Pages/Research/DER/PathogensandVectors/CCPlasmodiumComparativeWhitePaper0813.pdf.Google Scholar
Barsoum, R. (1998). Malarial nephropathies. Nephrology Dialysis Transplantation 13, 1588–1597.Google Scholar
Barsoum, R. S. (2000). Malarial acute renal failure. Journal of the American Society of Nephrology 11, 2147–2154.CrossRefGoogle ScholarPubMed
Coatney, G. R., Collins, W. E., Warren, M. and Contacos, P. G. (1971). The Primate Malarias, pp. 245–258. US Government Printing Office, Washington, DC, USA.Google Scholar
Collins, W. E. and Barnwell, J. W. (2009). Plasmodium knowlesi: finally being recognized. Journal of Infectious Diseases 199, 1107–1108.Google Scholar
Craig, A. G., Grau, G. E., Janse, C., Kazura, J. W., Milner, D., Barnwell, J. W. and participants of the Hinxton Retreat meeting on Animal Models for Research on Severe Malaria (2012). The role of animal models for research on severe malaria. PLOS Pathogens 8, e1002401.CrossRefGoogle ScholarPubMed
Gilles, H. M. and Hendrickse, R. G. (1960). Possible aetiological role of Plasmodium malariae in “nephrotic syndrome” in Nigerian children. Lancet i, 806–807.CrossRefGoogle Scholar
Gilles, H. M. and Hendrickse, R. G. (1963). Nephrosis in Nigerian children: role of Plasmodium malariae, and effect of antimalarial treatment. British Medical Journals 1, 27–31.CrossRefGoogle Scholar
Hedelius, R., Fletcher, J. J., Glass, W. F. II, Susanti, A. I. and Maguire, J. D. (2011). Nephrotic syndrome and unrecognized Plasmodium malariae infection in a US navy sailor 14 years after departing Nigeria. Journal of Travel Medicine 18, 288–291.CrossRefGoogle Scholar
Hendrickse, R. G. and Adeniyi, A. (1979). Quartan malarial nephrotic syndrome in children. Kidney International 16, 64–74.CrossRefGoogle ScholarPubMed
Hendrickse, R. G. and Gilles, H. M. (1963). The nephrotic syndrome and other renal diseases in children in western Nigeria. East African Medical Journal 40, 186–201.Google Scholar
Hendrickse, R. G., Adeniyi, A., Edington, G. M., Glasgow, E. F., White, R. H. and Houba, V. (1972). Quartan malarial nephritic syndrome. Collaborative clinicopathological study in Nigerian school children. Lancet 1, 1143–1149.Google Scholar
Herwaldt, B. L. (2001). Laboratory-acquired parasitic infections from accidental exposures. Clinical Microbiology Reviews 14, 659–688.Google Scholar
Houba, V. (1975). Immunopathology of nephropathies associated with malaria. Bulletin of the World Health Organization 52, 199–207.Google Scholar
Houba, V., Allison, A. C., Hendrickse, R. C., de Petris, S., Edington, G. M. and Adeniyi, A. (1970). Immune complex diseases. In Proceedings of the International Symposium on Immune Complex Diseases (ed. Bonomo, K. and Turk, J. L.), p. 23. Carlo Erba Foundation, Milan, Italy.Google Scholar
Houba, V., Allison, A. C., Adeniyi, A. and Houba, J. E. (1971). Immunoglobulin classes and complement in biopsies of Nigerian children with the nephrotic syndrome. Clinical and Experimental Immunology 8, 761–774.Google Scholar
Houba, V., Lambert, P. H., Voller, A. and Soyanwo, M. A. (1976). Clinical and experimental investigation of immune complexes in malaria. Clinical Immunology and Immunopathology 6, 1–12.CrossRefGoogle ScholarPubMed
Kibukamusoke, J. W. (1968). Nephrotic syndrome and chronic renal disease in the tropics. British Medical Journal 2, 33–35.CrossRefGoogle ScholarPubMed
Kibukamusoke, J. W., Hutt, M. S. R. and Wilks, N. E. (1967). The nephrotic syndrome in Uganda and its association with quartan malaria. Quarterly Journal of Medicine 36, 393–408.Google ScholarPubMed
Morel-Maroger, L., Saimot, A. G., Sloper, J. C., Woodrow, D. F., Adam, C., Niang, I. and Payet, M. (1975). ‘Tropical nephropathy’ and ‘tropical extramembranous glomerulonephritis’ of unknown aetiology in Senegal. British Medical Journal 1, 541–546.Google Scholar
Nimri, L. F. and Lanners, N. H. (1994). Immune complexes and nephropathies associated with Plasmodium inui infection in the rhesus monkey. American Journal of Tropical Medicine and Hygiene 51, 183–189.Google Scholar
Olowu, W. A., Adelusola, K. A., Adefehinti, O. and Oyetunji, T. G. (2010). Quartan malaria-associated childhood nephrotic syndrome: now a rare clinical entity in malaria endemic Nigeria. Nephrology, Dialysis, Transplantation 25, 794–801.Google Scholar
Sitprija, V. and Boonpucknavig, V. (1994). Renal involvement in parasitic diseases. In Renal Pathology with Clinical and Functional Correlations (ed. Tisher, C. and Brenner, B. M.), pp. 626–657. J. P. Lippincott Co., Philadelphia, PA, USA.Google Scholar
The Plasmodium Writing Group (2007). Comprehensive sequencing proposal for Plasmodium 1–28. http://www.genome.gov/pages/research/der/pathogensandvectors/plasmodiumwhitepaperv8.pdf.Google Scholar
van Marck, E. A. E., Abdurrahman, M. B., Edington, G. M. and Aliyu, R. A. (1983). Ultrastructural aspects of childhood nephrotic syndrome in Northern Nigeria. Annales de la Societe belge de medecine tropicale 63, 49–57.Google Scholar
van Velthuysen, M.-L. F. and Florquin, S. (2000). Glomerulopathy associated with parasitic infections. Clinical Microbiology Reviews 13, 55–66.Google Scholar
Vinetz, J. M., Li, J., McCutchan, T. F. and Kaslow, D. C. (1998). Plasmodium malariae infection in an asymptomatic 74-year-old Greek woman with splenomegaly. New England Journal of Medicine 338, 367–371.Google Scholar
Voller, A. (1974). Immunopathology of malaria. Bulletin of the World Health Organization 50, 177–186.Google Scholar
Voller, A., Draper, C. C., Shwe, T. and Hutt, M. S. R. (1971). Nephrotic syndrome in monkey infected with human quartan malaria. British Medical Journal 4, 208–210.Google Scholar
Voller, A., Davies, D. R. and Hutt, M. S. R. (1973). Quartan malarial infections in Aotus trivirgatus with special reference to renal pathology. British Journal of Experimental Pathology 54, 457–486.Google Scholar
Ward, P. A. and Kibukamusoke, J. W. (1969). Evidence for soluble immune complexes in the pathogenesis of the glomerulonephritis in quartan malaria. Lancet 1, 281–285.Google ScholarPubMed
Wing, A. J., Hutt, M. S. R. and Kibukamusoke, J. W. (1972). Progression and remission in the nephrotic syndrome associated with quartan malaria in Uganda. QJM 41, 273–289.Google ScholarPubMed
WHO Memorandum (1972). Immunopathology of nephritis in Africa. Bulletin of the World Health Organization 46, 387–396.Google Scholar