Investigations on anopheline mosquitoes close to the nest sites of chimpanzees subject to malaria infection in Ugandan Highlands

Malaria Journal

Volumn 11, Issue , 2012, Pages

  Krief, Sabrina ^a,b   Levrero, Florence ^c   Krief, Jean Michel ^b   Thanapongpichat, Supinya ^d   Imwong, Mallika ^d   Snounou, Georges ^e,f   Kasenene, John M ^g   Cibot, Marie ^a   Gantier, Jean Charles ^h  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b Projet Pour la Conservation des Grands Singes   (France)

^c UNIVERSITÉ JEAN MONNET   (France)

^d MAHIDOL UNIVERSITY   (Thailand)

^e Institut National de la Sant et de la Recherche Mdicale   (France)

^f SORBONNE UNIVERSITÉ   (France)

^g MAKERERE UNIVERSITY   (Uganda)

^h Facult de Pharmacie de Chtenay Malabry   (France)

Author keywords

Anopheles; Chimpanzee; Kibale National Park; Malaria; Nesting behaviour; Plasmodium

Indexed keywords

CARBON DIOXIDE;

ANIMAL EXPERIMENT; ANOPHELES; ANOPHELES DEMEILLONI; ANOPHELES IMPLEXUS; ANOPHELES VINCKEI; ARTICLE; CHIMPANZEE; CONTROLLED STUDY; DISEASE CARRIER; DISEASE TRANSMISSION; ECOLOGY; FEEDING; FEMALE; GENE AMPLIFICATION; HUMAN; HUMIDITY; MALARIA; METEOROLOGICAL PHENOMENA; NESTING; NONHUMAN; PLASMODIUM; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; SPECIES IDENTIFICATION; TOPOGRAPHY; UGANDA;

ANIMALS; ANOPHELES; DNA, PROTOZOAN; MALARIA; PLASMODIUM; POLYMERASE CHAIN REACTION; PRIMATE DISEASES;

EID: 84862230731     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-11-116     Document Type: Article

References (78)

1. Why do chimpanzees die in the forest? The challenges of understanding and controlling for wild ape health. Boesch C, Am J Primatol 2008 70 722 726 10.1002/ajp.20571 18523961
2. Ferber D, Human diseases threaten great apes. Science 2000 289 1277 1278
3. High variety of different simian T-Cell leukemia virus type 1 strains in chimpanzees (Pan troglodytes verus) of the Ta National Park, Cte d'Ivoire. Leendertz FH, Junglen S, Boesch C, Formenty P, Couacy-Hymann E, Courgnaud V, Pauli G, Ellerbrok E, J Virol 2004 78 4352 4356 10.1128/JVI.78.8.4352-4356.2004 15047848 (Pubitemid 38437238)
4. Pathogens as drivers of population declines: The importance of systematic monitoring in great apes and other threatened mammals. Leendertz FH, Pauli G, Maetz-Rensing K, Boardman W, Nunn C, Ellerbrok H, Jensen SA, Junglen S, Boesch C, Biol Conserv 2006 131 325 337 10.1016/j.biocon.2006.05.002 (Pubitemid 43849648)
5. A new Bacillus anthracis kills wild chimpanzees and gorilla in West and Central Africa. Leendertz FH, Yumlu S, Pauli G, Boesch C, Couacy-Hymann E, Vigilant L, Junglen S, Schenk S, Ellerbrok H, PLoS Pathog 2006 2 8 10.1371/journal.ppat.0020008 16738706
6. Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Goldberg TL, Gillespie TR, Rwego IB, Wheeler E, Estoff EL, Chapman CA, Biol Conserv 2007 135 511 517 10.1016/j.biocon.2006.10.048
7. Clinical and pathological manifestation of oesophagostomosis in African great apes. Does self-medication in wild apes influence disease progression? Krief S, Jamart A, Mah S, Leendertz FH, Mtz-Rensing K, Crespeau F, Bain O, Guillot J, J Med Primatol 2008 37 188 195 10.1111/j.1600-0684.2008.00285.x 18331558
8. Yaws disease in a wild gorilla population and its impact on the reproductive status of males. Levrro F, Gatti S, Gautier-Hion A, Mnard N, Am J Phys Anthropol 2007 132 568 575 10.1002/ajpa.20560 17274014 (Pubitemid 46474033)
9. Gorilla susceptibility to Ebola virus: The cost of sociality. Caillaud D, Levrro F, Cristescu R, Gatti S, Dewas M, Douadi M, Gautier-Hion A, Raymond M, Mnard M, Curr Biol 2006 16 489 491 10.1016/j.cub.2006.06.017
10. Pandemic human viruses cause decline of endangered great apes. Kndgen S, Khl H, N'Goran PK, Walsh PD, Schenk S, Ernst N, Biek R, Formenty P, Matz-Rensing K, Schweiger B, Junglen S, Ellerbrok H, Nitsche A, Briese T, Lipkin WI, Pauli G, Boesch C, Leendertz FH, Curr Biol 2008 18 260 264 10.1016/j.cub.2008.01.012 18222690
11. Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. Kaur T, Singh J, Tong S, Humphrey C, Clevender D, Tan W, Szekely B, Wang Y, Li Y, Muse EA, Kiyono M, Hanamura S, Inoue E, Nakamura M, Huffman MA, Jiang B, Nishida T, Am J Primatol 2008 70 755 765 10.1002/ajp.20565 18548512
12. On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from bonobos. Krief S, Escalante AA, Pacheco MA, Mugisha L, Andr C, Halbwax M, Fischer A, Krief JM, Kasenene JM, Crandfield M, Cornejo OE, Chavatte JM, Lin C, Letourneur F, Grner AC, McCutchan TF, Rnia L, Snounou G, PLoS Pathog 2010 6 1000765 10.1371/journal.ppat.1000765 20169187
13. Nodular worm infection in wild chimpanzees in Western Uganda: A risk for human health? Krief S, Vermeulen B, Lafosse S, Kasenene JM, Nieguitsila A, Berthelemy M, LHostis M, Bain O, Guillot J, PLoS Negl Trop Dis 2010 4 630 10.1371/journal.pntd.0000630 20300510
14. WHO, Malaria factsheet [ http://who.int/mediacentre/factsheets/fs094/en/ print.html ]
15. Garnham PPC, Malaria parasites and other haemosporidiae Oxford: Blaskwell Scientific Publications 1966
16. Coatney GR, Collins WE, Warren M, Contacos PG, The Primate Malarias Washington DC: GPO 1971
17. A new malaria agent in African Hominids. Ollomo B, Durand P, Prugnolle F, Douzery E, Arnathau C, Nkoghe D, Leroy E, Renaud F, PLoS Pathog 2009 5 1000446 10.1371/journal.ppat.1000446 19478877
18. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Prugnolle F, Durand P, Neel C, Ollomo B, Ayala FJ, Arnathau C, Etienne L, Mpoudi-Ngole E, Nkoghe D, Leroy E, Delaporte E, Peeters M, Renaud F, Proc Natl Acad Sci USA 2010 107 1458 1463 10.1073/pnas.0914440107 20133889
19. African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. Duval L, Fourment M, Nerrienet E, Rousset D, Sadeuh SA, Goodman SM, Andriaholinirin NV, Randrianarivelojosia M, Paul RE, Robert V, Ayala FJ, Ariey F, Proc Natl Acad Sci USA 2010 107 10561 10566 10.1073/pnas.1005435107 20498054
20. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, Ndjango JBN, Sanz CM, Morgan DB, Locatelli S, Gonder MK, Kranzusch PJ, Walsh PD, Delaporte E, Mpoudi-Ngole E, Georgiev AV, Muller MN, Shaw GM, Peeters M, Sharp PM, Rayner JC, Hahn BH, Nature 2010 467 420 425 10.1038/nature09442 20864995
21. Wild chimpanzees infected with 5 Plasmodium species. Kaiser M, Lwa A, Ulrich M, Ellerbrok H, Goffe AS, Blasse A, Zommers Z, Couacy-Hymann E, Babweteera F, Zuberbhler K, Metzger S, Geidel S, Boesch C, Gillespie TR, Leendertz FH, Emerg Infect Dis 2010 16 1956 1959 10.3201/eid1612.100424 21122230
22. Chimpanzee malaria parasites related to Plasmodium ovale in Africa. Duval L, Nerrienet E, Rousset D, Sadeuh Mba SA, Houze S, Fourment M, Le Bras J, Robert V, Ariey F, PLoS ONE 2009 4 5520 10.1371/journal.pone.0005520
23. Identification of Plasmodium malariae, a human malaria parasite, in imported chimpanzees. Hayakawa T, Arisue N, Udono T, Hirai H, Sattabongkot J, Toyama T, Tsuboi T, Horii T, Tanabe K, PLoS ONE 2009 4 7412 10.1371/journal. pone.0007412 19823579
24. Rainfall pattern, El Nio and malaria in Uganda. Kilian AHD, Langi P, Talisuna A, Kabagambe G, Trans R Soc Trop Med H 1999 93 22 23 10.1016/S0035-9203(99)90165-7 (Pubitemid 29123713)
25. Reappearance of falciparum malaria in central highland plateaux of Madagascar. Lepers JP, Deloron P, Fontenille D, Coulanges P, Lancet 1988 331 586 (Pubitemid 18060501)
26. Environnement et paludisme au Burundi: propos dune pidmie de paludisme dans une rgion montagneuse non endmique. Marimbu J, Ndayiragije A, Le Bras M, Chaperon J, Bull Soc Pathol Exot 1993 86 399 401 7819788
27. Effects and control of a highland malaria epidemic in Uasin Gishu District, Kenya. Some ES, E Afr Med J 1994 71 2 8
28. Services stretched as malaria reaches Kenyan highlands. Kigotho AW, Lancet 1997 350 422 9259666
29. Reemergence of epidemic malaria in the highlands of western Kenya. Malakooti MA, Biomndo K, Shanks GD, Emerg Infect Dis 1998 4 671 676 10.3201/eid0404.980422 9866748 (Pubitemid 28553696)
30. Highland malaria in Uganda: prospective analysis of an epidemic associated with El Nino. Lindblade KA, Walker ED, Onapa AW, Katungu J, Wilson ML, Trans R Soc Trop Med Hyg 1999 93 480 487 10.1016/S0035-9203(99)90344-9 10696401 (Pubitemid 29495828)
31. Early warning of malaria epidemics in African highlands using Anopheles (Diptera: Culicidae) indoor resting density. Lindblade KA, Walker ED, Wilson ML, J Med Entomol 2000 37 664 674 10.1603/0022-2585-37.5.664 11004777
32. The effects of climatic factors on the distribution and abundance of malaria vectors in Kenya. Minakawa N, Sonye G, Mogi M, Githeko A, Yan G, J Med Entomol 2002 39 833 841 10.1603/0022-2585-39.6.833 12495180 (Pubitemid 135693338)
33. Influence of host and larval habitat distribution on the abundance of African malaria vectors in western Kenya. Minakawa N, Seda P, Yan G, Am J Trop Med Hyg 2002 67 32 38 12363061 (Pubitemid 35034317)
34. Relationship between altitude and intensity of malaria transmission in the Usambara Mountains, Tanzania. Bodker R, Akida J, Shayo D, Kisinza W, Msangeni HA, Pedersen EM, Lindsay SW, J Med Entomol 2003 40 706 717 10.1603/0022-2585-40.5.706 14596287 (Pubitemid 37399546)
35. Spatial distribution patterns of malaria vectors and sample size determination in spatially heterogeneous environments: a case study in the west Kenyan highland. Zhou G, Minakawa N, Githeko A, Yan G, J Med Entomol 2004 41 1001 1009 10.1603/0022-2585-41.6.1001 15605637 (Pubitemid 39606422)
36. Aspilia spp. leaves: A puzzle in the feeding behavior of wild chimpanzees. Wrangham RW, Nishida T, Primates 1983 24 276 282 10.1007/BF02381090
37. Chimpanzee use of medicinal leaves. In Understanding Chimpanzees. Edited by Harvard University Press. Wrangham RW, Goodall J, Cambridge. Heltne PG, Marquardt LA 1989 22 37
38. Observations on the illness and consumption of a possibly medicinal plant Vernonia amygdalina (DEL.), by a wild chimpanzee in the Mahale Mountains National Park, Tanzania. Huffman MA, Seifu M, Primates 1989 30 51 63 10.1007/BF02381210
39. Antischistosomal activities of sesquiterpene lactones and steroid glucosides from Vernonia amygdalina, possibly used by wild chimpanzees against parasite-related diseases. Jisaka M, Kawanaka M, Sugiyama H, Takegawa K, Huffman MA, Ohigashi H, Koshimizu K, Biosci Biotech Bioch 1992 56 845 846 10.1271/bbb.56.845
40. Diversity of medicinal plants use by chimpanzees in the wild. In Chimpanzee Cultures. Edited by Harvard University Press. Huffman MA, Wrangham RW, Mass: Wrangham RW, McGrew WC, de Wall FB, Heltne PG 1994 129 148
41. Toward the chemical ecology of medicinal plant-use in chimpanzees: The case of Vernonia amygdalina (Del.). A plant used by wild chimpanzees possibly for parasite-related diseases. Ohigashi H, Huffman MA, Izutsu D, Koshimizu K, Kawanaka M, Sugiyama H, Kirby GC, Warhurst DC, Allen D, Wright CW, Phillipson D, Timon-David P, Delmas F, Elias R, Balansard G, J Chem Ecol 1994 20 541 553 10.1007/BF02059596 (Pubitemid 2070126)
42. Leaf-swallowing by chimpanzees, and its relationship to tapeworm infection. Wrangham RW, Am J Primatol 1995 37 297 303 10.1002/ajp.1350370404
43. Leaf swallowing by chimpanzees, a behavioral adaptation for the control of strongyle nematode infections. Huffman MA, Page JE, Sukhdeo MVK, Gotoh S, Kalunde MS, Chandrasiri T, Towers GHN, Int J Primatol 1996 72 475 503 (Pubitemid 26352009)
44. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Huffman MA, Gotoh S, Turner L, Yoshida K, Primates 1997 38 111 125 10.1007/BF02382002
45. Self-induced increase of gut mobility and the control of parasitic infections in wild chimpanzees. Huffman MA, Caton JM, Int J Primatol 2001 22 329 346 10.1023/A:1010734310002 (Pubitemid 32579506)
46. Bioactive properties of plants ingested by chimpanzees (Pan troglodytes schweinfurthii) in the Kibale National Park, Uganda. Krief S, Huffman M, Svenet T, Hladik CM, Grellier P, Loiseau P, Wrangham RW, Am J Primatol 2006 68 51 71 10.1002/ajp.20206 16419122
47. Diversity of items of low nutritional value ingested by chimpanzees from Kanyawara, Kibale National Park, Uganda: an example of the etho-ethnology of chimpanzees. Krief S, Wrangham RW, Lestel D, Soc Sci Inform 2006 45 227 263 10.1177/0539018406063642 (Pubitemid 43679961)
48. Novel antimalarial compounds isolated after the survey of self-medicative behavior of wild chimpanzees in Uganda. Krief S, Martin M-T, Grellier P, Kasenene J, Sévenet T, Antimicrob Agents Chemother 2004 3196 3199 (Pubitemid 38989204)
49. Geophagy: soil consumption enhances the bioactivities of plants eaten by chimpanzees (Pan troglodytes schweinfurthii). Klein N, Frhlich F, Krief S, Naturwissenschaften 2008 95 325 331 10.1007/s00114-007-0333-0 18188538
50. A parasite resembling P. falciparum in a chimpanzee. Blacklock B, Adler S, Ann Trop Med Parasit 1922 16 99 106
51. Les Plasmodium des anthropodes de lAfrique Centrale et leurs relations avec les Plasmodium humains. Rodhain J, Bull Acad Roy Med Belgique 1941 6 21 60
52. Studies on malaria in chimpanzees. III Gametogony of Plasmodium reichenowi. Bray RS, Ann Soc Belge Med Trop 1957 37 169 174 13459024
53. Malaria hotspot areas in a highland Kenya site are consistent in epidemic and non-epidemic years and are associated with ecological factors. Ernst KC, Adoka SO, Kowuor DO, Wilson ML, John CC, Malar J 2006 5 78 10.1186/1475-2875-5- 78 16970824 (Pubitemid 44496276)
54. Vocalizations, phylogeny and palaeogeography of red Colobus monkeys (Colobus badius). Struhsaker TT, Afr J Ecol 1981 19 265 283 10.1111/j.1365-2028. 1981.tb01064.x
55. Habitat alteration and the conservation of African primates: case study of Kibale National Park, Uganda. Chapman CA, Lambert JE, Am J Primat 2000 50 169 185 10.1002/(SICI)1098-2345(200003)50:3<169::AID-AJP1>3.0.CO;2-P (Pubitemid 30149506)
56. Range use of the forest chimpanzees of Kibale: Implications for the evolution of chimpanzee social organization. Chapman CA, Wrangham RW, Am J Primatol 1993 31 263 273 10.1002/ajp.1350310403
57. Predicting patterns of crop damage by wildlife around Kibale National Park, Uganda. Naughton-Treves L, Conserv Biol 1998 12 156 168 10.1046/j.1523-1739.1998.96346.x (Pubitemid 28153814)
58. Yeast-generated CO2 as a convenient source of carbon dioxide for adult mosquito sampling. Saitoh Y, Hattori J, Chinone S, Nihei N, Tsuda Y, Kurahashi H, Kobayashi M, J Am Mosquito Contr Assoc 2004 20 261 264 (Pubitemid 41322549)
59. The role of carbon dioxide in host-finding by mosquitoes (Diptera: Culicidae): a review. Gillies MT, Bull Entomol Res 1980 70 525 532 10.1017/S0007485300007811
60. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region), 2nd ed. Gillies MT, De Meillon B, South Afr Inst med Res Publ 1968 54 1 343
61. Nested PCR analysis of Plasmodium parasites. Snounou G, Singh B, Methods Mol Med 2002 72 189 203 12125116
62. Comparison of CDC miniature light traps and human biting collections for mosquito catches during malaria vector surveys in peninsular Malaysia. Parsons RE, Dondero TJ, Hooi CW, Mosq News 1974 34 211 213
63. The use of light traps for long-term surveillance of mosquitoes of epidemiological importance on the Kano Plain, Kenya. Chandler JA, Hill MN, Highton RB, East Afr Med J 1976 53 596 600 13987 (Pubitemid 8024798)
64. Variation in malaria transmission intensity in seven sites throughout Uganda. Okello PE, Van Bortel W, Byaruhanga AM, Correwyn A, Roelants P, Talisuna A, D'Alessandro U, Coosemans M, Am J Trop Med Hyg 2006 75 219 225 16896122 (Pubitemid 46941334)
65. Anopheles paludis, vecteur important du paludisme au Zare. Karch S, Mouchet J, Bull Soc Pathol Exot 1992 85 388 389 1292800
66. Notes entomologiques (Diptera: Anophelinae). III. Parent M, Vincke I, Rec Sci Med Congo Belge 1945 4 23 24
67. Anopheles (Christya) implexus, Theobald. Description de la varit locale de la valle du Mosso (Urundi). Lambrecht FL, Rev Zool Bot Afr 1954 50 204 209
68. Studies on malaria in Southern Nigeria. Barber MA, Olinger MT, Ann Trop Med Parasit 1931 25 461
69. The mosquitoes of Bwamba County, Uganda. VIII. Records of occurrence, behaviour and habitat. Haddow AJ, Van Someren ECC, Lumsden WHR, Harper Jo, Gillet JD, Bull Ent Res 1951 42 207 10.1017/S0007485300025311
70. The mosquitoes of Zaria Province. Hanney PW, Northern Nigeria. Bull Ent Res 1960 51 145
71. Hervy JP, Le Goff G, Geoffrey B, Herve JP, Manga L, Brunhes J, Les Anophles de la rgion afrotropicale, Logiciel didentification et denseignement trilingue Paris: ORSTOM/OCEAC 1998
72. Spatial clustering of malaria and associated risk factors during an epidemic in a highland area of western Kenya. Brooker S, Clarke S, Njagi JK, Polack S, Mugo B, Estambale B, Muchiri E, Magnussen P, Cox J, Trop Med Int Health 2004 9 757 766 10.1111/j.1365-3156.2004.01272.x 15228485 (Pubitemid 38962002)
73. Botanical and topographical factors influencing nesting-site selection by chimpanzees in Kalinzu Forest, Uganda. Furuichi T, Hashimoto C, Int J Primatol 2004 25 755 765 (Pubitemid 39008936)
74. Sources of variation in the nesting behavior of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest. Brownlow AR, Plumptre AJ, Reynolds V, Ward R, Am J Primatol 2001 55 49 55 10.1002/ajp.1038 11536316 (Pubitemid 32818371)
75. Do chimpanzees build comfortable nests? Stewart FA, Pruetz JD, Hansell MH, Am J Primatol 2007 69 930 939 10.1002/ajp.20432 17358021 (Pubitemid 47280333)
76. Comparison of nests made by different populations of chimpanzees. Baldwin PJ, Sabaster PJ, McGrew WC, Tutin CEG, Primates 1981 22 474 486 10.1007/BF02381239
77. Sylvatic transmission of arboviruses among Bornean orangutans. Wolfe ND, Kilbourn AM, Karesh WB, Rahman HA, Bosi EJ, Cropp BC, Andau M, Spielman A, Gubler DJ, Am J Trop Med Hyg 2001 64 310 316 11463123
78. Chapman CA, Chapman LJ, Zanne AE, Poulsen JR, Clark CJ, A 12-year phenological record of fruiting: Implications for frugivore populations and indicators of climate change In Tropical Fruits and Frugivores. Edited by Dew JL,Boubli J. Netherlands: Springer 2005 75 92