No measurable adverse effects of Lassa, Morogoro and Gairo arenaviruses on their rodent reservoir host in natural conditions

Parasites and Vectors

Volumn 10, Issue 1, 2017, Pages

  Mariën, Joachim ^a   Borremans, Benny ^a,e   Gryseels, Sophie ^a,f   Soropogui, Barré ^b   De Bruyn, Luc ^a   Bongo, Gédéon Ngiala ^c,g   Becker Ziaja, Beate ^c   De Bellocq, Joëlle Goüy ^d   Günther, Stephan ^c   Magassouba, N’Faly ^b   Leirs, Herwig ^a   Fichet Calvet, Elisabeth ^c  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b centre hospitalier et universitaire de Conakry   (Guinea)

^c BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^d INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f University of Arizona   (United States)

^g UNIVERSITY OF KINSHASA   (Congo)

Author keywords

Arenavirus; Gairo virus; Host pathogen interaction; Lassa virus; Mastomys natalensis; Morogoro virus; Reservoir host; Rodent borne disease

Indexed keywords

ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARENAVIRUS INFECTION; ARTICLE; AUTOPSY; BODY CONSTITUTION; BODY HEIGHT; BODY MASS; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE TRANSMISSION; FEMALE; HUMAN; IMMUNOFLUORESCENCE TEST; LASSA VIRUS; MALE; MASTOMYS NATALENSIS; MOROGORO AND GAIRO ARENAVIRUS; NONHUMAN; PATHOGENICITY; PROBABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RODENT; SEXUAL MATURITY; VIRUS HEMORRHAGIC FEVER; ZOONOSIS; ANIMAL; ARENAVIRIDAE; DISEASE CARRIER; GUINEA; HETEROZYGOTE; ISOLATION AND PURIFICATION; MURINE; PATHOLOGY; PHYSIOLOGY; TANZANIA; VETERINARY; VIROLOGY;

ANIMALS; ARENAVIRIDAE INFECTIONS; ARENAVIRUS; CARRIER STATE; DISEASE VECTORS; GUINEA; MURINAE; TANZANIA;

EID: 85018173774     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/s13071-017-2146-0     Document Type: Article

References (66)

1. Monath TP, Newhouse VF, Kemp GE, Setzer HWCA. Lassa virus isolation from Mastomys natalensis rodents during an epidemic in Sierra Leone. Science. 1974;185:263-5.
2. Gryseels S, Rieger T, Oestereich L, Cuypers B, Borremans B, Makundi R, et al. Gairo virus, a novel arenavirus of the widespread Mastomys natalensis: Genetically divergent, but ecologically similar to Lassa and Morogoro viruses. Virology. 2015;476:249-56.
3. Gryseels S, Baird S, Borremans B, Makundi R, Leirs H, Goüy de Bellocq J. When viruses don’t go viral: the importance of host phylogeographic structure in the spatial spread of arenaviruses. PLoS Pathog. 2017;13:1.
4. Olayemi A, Obadare A, Oyeyiola A, Igbokwe J, Fasogbon A, Igbahenah F, et al. Arenavirus diversity and phylogeography of Mastomys natalensis rodents, Nigeria. Emerg Infect Dis. 2016;22:694-7.
5. Günther S, Hoofd G, Charrel R, Röser C, Becker-Ziaja B, Lloyd G, et al. Mopeia virus-related arenavirus in Natal multimammate mice, Morogoro, Tanzania. Emerg Infect Dis. 2009;15:2008-12.
6. Wulff H, McIntosh BM, Hamner DB, Johnson KM. Isolation of an arenavirus closely related to Lassa virus from Mastomys natalensis in south-east Africa. Bull World Health Organ. 1977;55:441-4.
7. Ishii A, Thomas Y, Moonga L, Nakamura I, Ohnuma A, Hang’ombe B, et al. Novel arenavirus, Zambia. Emerg Infect Dis. 2011;17:1921-4.
8. McCormick JB. Lassa fever. In: Saluzzo JF, Dodet B, editors. Emergence and Control of Rodent-Borne Viral Diseases. Berlin: Elsevier; 1999. p. 177-95.
9. Monath TP. Lassa fever: New issues raised by field studies in West Africa. J Infect Dis. 1987;155:433-6.
10. World Health Organization: WHO fact sheet. http://www.who.int/csr/disease/lassafever/en/). Accessed 23 Apr 2017.
11. Walker DH, Murphy FA. Pathology and pathogenesis of arenavirus infections. Curr Top Microbiol Immunol. 1987;133:89-113.
12. Günther S, Lenz O. Lassa virus. Crit Rev Clin Lab Sci. 2004;41:339-90.
13. Anderson RM, May R. Population biology of infectious diseases: Part II. Nature. 1979;280:361-7.
14. Anderson RM, May RM. Coevolution of host and parasites. Parasitology. 1982;85:411-26.
15. Frank S. Models of parasite virulence. Q Rev Biol. 1996;71:37-78.
16. Alizon S, Hurford A, Mideo N, Van Baalen M. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J Evol Biol. 2009;22:245-59.
17. Knell RJ. Syphilis in renaissance Europe: rapid evolution of an introduced sexually transmitted disease? Proc Biol Sci. 2004;271(Suppl):S174-6.
18. Dwyer G, Levin S, Buttel L. A simulation model of the population dynamics and evolution of myxomatosis. Ecol. Monogr. 1990;60(4):423-47
19. Kerber R, Rieger T, Busch C, Flatz L, Pinschewer DD, Kümmerer BM, et al. Cross-species analysis of the replication complex of Old World arenaviruses reveals two nucleoprotein sites involved in L protein function. J Virol. 2011;85:12518-28.
20. Childs JE, Peters CJ. Ecology and epidemiology of arenaviruses and their hosts. In: Salvato MS, editor. The Arenaviridae. New York: Plenum Press; 1993. p. 331-85.
21. Oldstone M. Arenaviruses: biology and immunotherapy. In: Clarke P, editor. Current topics in microbiology and immunology. New York: Springer Verlag; 2002. p. 1-142.
22. Hotchin JE, Cinits M. Lymphocytic choriomeningitis infection of mice as a model for the study of latent virus infection1. Can J Microbiol. 1958;4:149-63.
23. Oldstone M, Dixon F. Susceptibility of different mouse strains to lymphocytic choriomeningitis virus. J Immunol. 1968;100:355-7.
24. Mims CA. Observations on mice infected congenitally or neonatally with lymphocytic choriomeningitis. Arch. Virol. 1970;30(1):67-74.
25. Oldstone M, Sinha Y, Blount P, Tishon A, Rodriguez M, von Wedel R, et al. Virus-induced alterations in homeostasis: Alterations in differentiated functions of infected cells in vivo. Science. 1982;218:6.
26. Webb P, Justines G, Johnson K. Infection of wild and laboratory animals with Machupo and Latino viruses. Bull World Health Organ. 1975;52:493-9.
27. Vitullo A, Hodara V, Merani MS. Effect of persistent infection with Junin virus on growth and reproduction of its natural reservoir, Calomys musculinus. Am J Trop Med Hyg. 1987;37:663-9.
28. Vitullo A, Merani MS. Vertical transmission of Junin virus in experimentally infected adult Calomys musculinus. Intervirology. 1990;31:339-44.
29. Borremans B, Vossen R, Becker-ziaja B, Gryseels S, Hughes N, Van Gestel M, et al. Shedding dynamics of Morogoro virus, an African arenavirus closely related to Lassa virus, in its natural reservoir host Mastomys natalensis. Sci Rep. 2015;5:10445.
30. Walker DH, Wulff H, Lange JV, Murphy FA. Comparative pathology of Lassa virus infection in monkeys, guinea-pigs, and Mastomys natalensis. Bull World Health Organ. 1975;52:523-34.
31. Demartini J, Green D, Monath TP. Lassa virus infection in Mastomys natalensis in Sierra Leone: Gross and microscopic findings in infected and uninfected animals. Bull World Health Organ. 1975;52:651-63.
32. Lalis A, Evin A, Janier M, Koivogui L, Denys C. Host evolution in Mastomys natalensis (Rodentia: Muridae): an integrative approach using geometric morphometrics and genetics. Integr Zool. 2015;10:505-14.
33. Leirs H, Stuyck J, Verhagen R, Verheyen W. Seasonal variation in growth of Mastomys natalensis (Rodentia: Muridae) in Morogoro, Tanzania. Afr J Ecol. 1990;28:298-306.
34. Demby AH, Inapogui A, Kargbo K, Koninga J, Kourouma K, Kanu J, et al. Lassa fever in Guinea: II. Distribution and prevalence of Lassa virus infection in small mammals. 2001;1:283-99.
35. Borremans B, Leirs H, Gryseels S, Günther S, Makundi R, Goüy de Bellocq J. Presence of Mopeia virus, an African arenavirus, related to biotope and individual rodent host characteristics: implications for virus transmission. Vector Borne Zoonotic Dis. 2011;11:1125-31.
36. Kallio ER, Helle H, Koskela E, Mappes T, Vapalahti O. Age-related effects of chronic hantavirus infection on female host fecundity. J Anim Ecol. 2015;84:1264-72.
37. Lord RD. The lens as an indicator of age in cottontail rabbits. J Wildl Manage. 1959;23:358-60.
38. Morris P. A review of mammalian age determination methods. Mamm Rev. 1972;2:69-104.
39. Leirs H. Population ecology of Mastomys natalensis (Smith, 1834). Implications for rodent control in Africa. Brussels: Belgian Administration for Development Cooperation; 1995. Agricultural edition 35: 1994.
40. Augusteyn RC. Growth of the eye lens : I. Weight accumulation in multiple species. Mol Vis. 2014;20:410-26.
41. Jánová E, Nesvadbová J, Tkadlec E. Is the eye lens method of age estimation reliable in voles? Folia Zool. 2007;52:119-25.
42. Fichet-Calvet E, Lecompte E, Koivogui L, Soropogui B, Doré A, Kourouma F, et al. Fluctuation of abundance and Lassa virus prevalence in Mastomys natalensis in Guinea, West Africa. Vector Borne Zoonotic Dis. 2007;7:119-28.
43. Fichet-Calvet E, Lecompte E, Koivogui L, Daffis S, ter Meulen J. Reproductive characteristics of Mastomys natalensis and Lassa virus prevalence in Guinea, West Africa. Vector Borne Zoonotic Dis. 2008;8:41-8.
44. Fichet-Calvet E, Becker-Ziaja B, Koivogui L, Günther S. Lassa serology in natural populations of rodents and horizontal transmission. Vector Borne Zoonotic Dis. 2014;14:665-74.
45. Fichet-Calvet E, Ölschläger S, Strecker T, Koivogui L, Becker-Ziaja B, Camara AB, et al. Spatial and temporal evolution of Lassa virus in the natural host population in Upper Guinea. Sci Rep. 2016;6:1-6.
46. Vieth S, Drosten C, Lenz O, Vincent M, Omilabu S, Hass M, et al. RT-PCR assay for detection of Lassa virus and related Old World arenaviruses targeting the L gene. Trans R Soc Trop Med Hyg. 2007;101:1253-64.
47. Olschläger S, Lelke M, Emmerich P, Panning M, Drosten C, Hass M, et al. Improved detection of Lassa virus by reverse transcription-PCR targeting the 5′ region of S RNA. J Clin Microbiol. 2010;48:2009-13.
48. Wulff H, Lange J. Indirect immunofluorescence for the diagnosis of Lassa fever infection. Bull World Health Organ. 1975;52:429-36.
49. Hufert FT, Liidke W, Sehmitz H. Epitope mapping of the Lassa virus nucleoprotein using monoclonal anti-nucleocapsid antibodies. Arch Virol. 1989;106:201-12.
50. R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2016. http://www.r-project.org. Accessed 12 Dec.
51. Bernshtein A, Apekina N, Mikhailova T, Myasnikov Y, Khlyap L, Korotkov Y, et al. Dynamics of Puumala hantavirus infection in naturally infected bank voles (Clethrinomys glareolus). Arch Virol. 1999;144:2415-28.
52. Verhagen R, Leirs H, Tkachenko E, van der Groen G. Ecological and epidemiological data on hantavirus in bank vole populations in Belgium. Arch Virol. 1986;91:193-205.
53. Kallio ER, Poikonen A, Vaheri A, Vapalahti O, Henttonen H, Koskela E, et al. Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proc Biol Sci. 2006;273:2771-6.
54. Kallio ER, Voutilainen L, Vapalahti O, Vaheri A, Henttonen H, Mappes T, et al. Endemic hantavirus infection impairs the winter survival of its rodent host. Ecology. 2007;88(8):1911-6.
55. Tersago K, Crespin L, Verhagen R, Leirs H. Impact of Puumala virus infection on maturation and survival in bank voles: a capture-mark-recapture analysis. J Wildl Dis. 2012;48:148-56.
56. Voutilainen L, Sironen T, Tonteri E, Tuiskunen Bäck A, Razzauti M, Karlsson M, et al. Life-long shedding of Puumala hantavirus in wild bank voles (Myodes glareolus). J Gen Virol. 2015;96:1238-47.
57. Barber I, Dingemanse NJ. Parasitism and the evolutionary ecology of animal personality. Philos Trans R Soc Lond B Biol Sci. 2010;365:4077-88.
58. Sluydts V, Crespin L, Davis S, Lima M, Leirs H. Survival and maturation rates of the African rodent, Mastomys natalensis: density-dependence and rainfall. Integr Zool. 2007;2:220-32.
59. Goyens J, Reijniers J, Borremans B, Leirs H. Density thresholds for Mopeia virus invasion and persistence in its host Mastomys natalensis. J Theor Biol. 2013;317:55-61.
60. Vitullo A, Merani M. Is vertical transmission sufficient to maintain Junin virus in nature? J Gen Virol. 1988;69:1437-40. 56. 57.
61. Veenstra AJF. The behaviour of the multimammate mouse, Rattus (Mastomys) natalensis (A. Smith). Anim Behav. 1958;6:195-206.
62. Kennis J, Sluydts V, Leirs H, van Hooft WFP. Polyandry and polygyny in an African rodent pest species, Mastomys natalensis. Mammalia. 2008;72:150-60.
63. Voutilainen L, Kallio ER, Niemimaa J, Vapalahti O, Henttonen H. Temporal dynamics of Puumala hantavirus infection in cyclic populations of bank voles. Sci Reports. 2016;6:1-14.
64. Sauvage F, Langlais M, Yoccoz NG, Pontier D. Modelling hantavirus in fluctuating populations of bank voles: the role of indirect transmission on virus persistence. J Anim Ecol. 2003;72:1-13.
65. Carlos J, Torre D, Oldstone M. Selective disruption of growth hormone transcription machinery by viral infection. Proc Natl Acad Sci U S A. 1992;89:9939-43.
66. Oldstone M, Southern P, Rodriquez M, Lampert P. Virus persists in beta cells of islets of Langerhans and is associated with chemical manifestations of diabetes. Science. 1984;224:1440-3.