1921
Volume 94, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract

Serological markers, combined with spatial analysis, offer a comparatively more sensitive means by which to measure and detect foci of malaria transmission in highland areas than traditional malariometric indicators. parasite prevalence, seroprevalence, and seroconversion rate to merozoite surface protein-1 (MSP-1) were measured in a cross-sectional survey to determine differences in transmission between altitudinal strata. Clusters of parasite prevalence and high antibody responses to MSP-1 were detected and compared. Results show that prevalence and seroprevalence generally decreased with increasing altitude. However, transmission was heterogeneous with hotspots of prevalence and/or seroprevalence detected in both highland and highland fringe altitudes, including a serological hotspot at 2,200 m. Results demonstrate that seroprevalence can be used as an additional tool to identify hotspots of malaria transmission that might be difficult to detect using traditional cross-sectional parasite surveys or through vector studies. Our study findings identify ways in which malaria prevention and control can be more effectively targeted in highland or low transmission areas via serological measures. These tools will become increasingly important for countries with an elimination agenda and/or where malaria transmission is becoming patchy and focal, but receptivity to malaria transmission remains high.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.15-0653
2016-06-01
2017-11-22
Loading full text...

Full text loading...

/deliver/fulltext/14761645/94/6/1251.html?itemId=/content/journals/10.4269/ajtmh.15-0653&mimeType=html&fmt=ahah

References

  1. Cox JS, Craig MH, Le Sueur D, Sharp BL, , 1999. Mapping Malaria Risk in the Highlands of Africa. Durban, South Africa: MARA/HIMAL.
  2. Drakeley CJ, Carneiro I, Reyburn H, Malima R, Lusingu JP, Cox J, Theander TG, Nkya WMMM, Lemnge MM, Riley EM, , 2005. Altitude-dependent and -independent variations in Plasmodium falciparum prevalence in northeastern Tanzania. J Infect Dis 191: 15891598.[Crossref]
  3. Jelliffe DB, Karrach HA, Bennett FJ, Stroud CE, Novotny ME, Musoke LK, Jelliffe EFP, , 1961. Field survey of the health of Bachiga children in the Kayonza district of Kigezi, Uganda. Am J Trop Med Hyg 10: 435445.
  4. Kilian AHD, , 1995. Malaria control in Kabarole and Bundibugyo Districts, Western Uganda. Report on a comprehensive malaria situation analysis and design of a district control programme, March 14–15, 1995, Fort Portal, Uganda.
  5. Okello P, Van Bortel W, Byaruhanga A, Correwyn A, Roelants P, Talisuna A, D'Alessandro U, Coosemans M, , 2006. Variation in malaria transmission intensity in seven sites throughout Uganda. Am J Trop Med Hyg 75: 219225.
  6. Kristan M, Abeku TA, Beard J, Okia M, Rapuoda B, Sang J, Cox J, , 2008. Variations in entomological indices in relation to weather patterns and malaria incidence in east African highlands: implications for epidemic prevention and control. Malar J 7: 231.[Crossref]
  7. Brooker S, Clarke S, Njagi JK, Polack S, Mugo B, Estambale B, Muchiri E, Magnussen P, Cox J, , 2004. Spatial clustering of malaria and associated risk factors during an epidemic in a highland area of western Kenya. Trop Med Int Health 9: 757766.[Crossref]
  8. Ernst KC, Adoka SO, Kowuor DO, Wilson ML, John CC, , 2006. Malaria hotspot areas in a highland Kenya site are consistent in epidemic and non-epidemic years and are associated with ecological factors. Malar J 5: 78.[Crossref]
  9. Roberts JM, , 1964. The control of epidemic malaria in the highlands of western Kenya. Part II. The campaign. J Trop Med Hyg 61: 191199.
  10. Peterson I, Borrell LN, El-Sadr W, Teklehaimanot A, , 2009. Individual and household level factors associated with malaria incidence in a highland region of Ethiopia: a multilevel analysis. Am J Trop Med Hyg 80: 103111.
  11. Minakawa N, Omukunda E, Zhou G, Githeko A, Yan G, , 2006. Malaria vector productivity in relation to the highland environment in Kenya. Am J Trop Med Hyg 75: 448453.
  12. Minakawa N, Munga S, Atieli F, Mushinzimana E, Zhou G, Githeko AK, Yan G, , 2005. Spatial distribution of anopheline larval habitats in western Kenyan highlands: effects of land cover types and topography. Am J Trop Med Hyg 73: 157165.
  13. Munga S, Minakawa N, Zhou G, Mushinzimana E, Barrack OOJ, Githeko AK, Yan G, , 2006. Association between land cover and habitat productivity of malaria vectors in western Kenyan highlands. Am J Trop Med Hyg 74: 6975.
  14. Ndenga B, Githeko A, Omukunda E, Munyekenye G, Atieli H, Wamai P, Mbogo C, Minakawa N, Zhou G, Yan G, , 2006. Population dynamics of malaria vectors in western Kenya highlands. J Med Entomol 43: 200206.[Crossref]
  15. Bousema T, Drakeley C, Gesase S, Hashim R, Magesa S, Mosha F, Otieno S, Carneiro I, Cox J, Msuya E, Kleinschmidt I, Maxwell C, Greenwood B, Riley E, Sauerwein R, Chandramohan D, Gosling R, , 2010. Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis 201: 17641774.[Crossref]
  16. Kreuels B, Kobbe R, Adjei S, Kreuzberg C, von Reden C, Bäter K, Klug S, Busch W, Adjei O, May J, , 2008. Spatial variation of malaria incidence in young children from a geographically homogeneous area with high endemicity. J Infect Dis 197: 8593.[Crossref]
  17. Carter R, Mendis KN, Roberts D, , 2000. Spatial targeting of interventions against malaria. Bull World Health Organ 78: 14011411.
  18. Clark R, , 2009. Embryotoxicity of the artemisinin antimalarials and potential consequences for use in women in the first trimester. Reprod Toxicol 28: 285296.[Crossref]
  19. Kelly M, , 1964. Terminology of malaria and of malaria eradication. Lancet 1: 157158.
  20. Bautista CT, Chan AST, Ryan JR, Calampa C, Roper MH, Hightower AW, Magill AJ, , 2006. Epidemiology and spatial analysis of malaria in the northern Peruvian Amazon. Am J Trop Med Hyg 75: 12161222.
  21. Gaudart J, Poudiougou B, Dicko A, Ranque S, Toure O, Sagara I, Diallo M, Diawara S, Ouattara A, Diakite M, Doumbo OK, , 2006. Space-time clustering of childhood malaria at the household level: a dynamic cohort in a Mali village. BMC Public Health 6: 286.[Crossref]
  22. Smith DL, McKenzie FE, Snow RW, Hay SI, , 2007. Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biol 5: e42.[Crossref]
  23. Tusting LS, Bousema T, Smith DL, Drakeley C, , 2014. Measuring changes in Plasmodium falciparum transmission: precision, accuracy and costs of metrics. Adv Parasitol 84: 151208.[Crossref]
  24. Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SLR, Carneiro I, Malima R, Lusingu J, Manjurano A, Nkya WM, Lemnge MM, Cox J, Reyburn H, Riley EM, , 2005. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci USA 102: 51085113.[Crossref]
  25. Corran P, Coleman P, Riley E, Drakeley C, , 2007. Serology: a robust indicator of malaria transmission intensity? Trends Parasitol 23: 575582.[Crossref]
  26. Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, Griffin J, Cox J, Abeku T, Bousema T, Ghani AC, Drakeley C, Riley E, , 2008. Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malar J 7: 195.[Crossref]
  27. Lynch CA, Bruce J, Bhasin A, Roper C, Cox J, Abeku TA, , 2015. Association between recent internal travel and malaria in Ugandan highland and highland fringe areas. Trop Med Int Health 20: 773780.[Crossref]
  28. Cook J, Reid H, Iavro J, Kuwahata M, Taleo G, Clements A, McCarthy J, Vallely A, Drakeley C, , 2010. Using serological measures to monitor changes in malaria transmission in Vanuatu. Malar J 9: 169.[Crossref]
  29. Kulldorf M, Nagarwalla N, , 1995. Spatial disease clusters: detection and inference. Stat Med 14: 799810.[Crossref]
  30. Kulldorff M, , 1997. A spatial scan statistic. Commun Stat Theory Methods 26: 14811496.[Crossref]
  31. Naus JI, , 1965. The distribution of the size of the maximum cluster of points on a line. J Am Stat Assoc 60: 532538.[Crossref]
  32. Wilson S, Booth M, Jones FM, Mwatha JK, Kimani G, Kariuki HC, Vennervald BJ, Ouma JH, Muchiri E, Dunne DW, , 2007. Age-adjusted Plasmodium falciparum antibody levels in school-aged children are a stable marker of microgeographical variations in exposure to Plasmodium infection. BMC Infect Dis 7: 67.[Crossref]
  33. Yeka A, Nankabirwa J, Mpimbaza A, Kigozi R, Arinaitwe E, Drakeley C, Greenhouse B, Kamya MR, Dorsey G, Staedke SG, , 2015. Factors associated with malaria parasitemia, anemia and serological responses in a spectrum of epidemiological settings in Uganda. PLoS One 10: e0118901.[Crossref]
  34. Bejon P, Williams TN, Liljander A, Noor AM, Wambua J, Ogada E, Olotu A, Osier FHA, Hay SI, Färnert A, Marsh K, , 2010. Stable and unstable malaria hotspots in longitudinal cohort studies in Kenya. PLoS Med 7: e1000304.[Crossref]
  35. Mosha JF, Sturrock HJW, Greenwood B, Sutherland CJ, Gadalla NB, Atwal S, Hemelaar S, Brown JM, Drakeley C, Kibiki G, Bousema T, Chandramohan D, Gosling RD, , 2014. Hot spot or not: a comparison of spatial statistical methods to predict prospective malaria infections. Malar J 13: 53.[Crossref]
  36. Garnham PCC, , 1948. The incidence of malaria at high altitudes. J Natl Malar Soc 7: 275284.
  37. de Zulueta J, Kafuko GW, Cullen JR, , 1963. An investigation of the annual cycle of malaria in Masaka District (Uganda). East Afr Med J 40: 469488.
  38. De Rook H, Cullen JR, , 1957. Unpublished Report of the WHO Malaria Survey of the Resettlement Area, North Kigezi District, Uganda.
  39. Balls MJ, Bødker R, Thomas CJ, Kisinza W, Msangeni HA, Lindsay SW, , 2004. Effect of topography on the risk of malaria infection in the Usambara Mountains, Tanzania. Trans R Soc Trop Med Hyg 98: 400408.[Crossref]
  40. Gill C, , 1923. The relation of malaria to altitude. Indian J Med Res 11: 511542.
  41. Uganda Bureau of Statistics (UBOS) and ICF Macro, 2010. Uganda Malaria Indicator Survey 2009. Calverton, MD: UBOS and ICF Macro.
  42. Jelliffe E, Jelliffe D, , 1963. Plasmodium malariae in Ugandan children: I Prevalence in young children in rural communities. Am J Trop Med Hyg 12: 296297.
  43. Brown RE, Wilks NE, Allen DM, , 1970. Health survey of primary schoolchildren in Uganda: incidence of anaemia, splenomegaly, hookworm and malaria. East Afr Med J 47: 302318.
  44. de Zulueta J, , 1959. Kigezi Malaria Report. Kampala, Uganda: WHO/AFRO.
  45. Uganda Protectorate. Annual Medical and Sanitary Reports, 1917–1951. Entebbe, Uganda: Entebbe Government Printers.
  46. Langi P, Lalobo O, Mpeka B, Mpigika G, , 1994. Malaria Situation Analysis in Apac, Kampala and Rukungiri Districts, Uganda. Entebbe, Uganda: Ministry of Health and United Nations Children's Fund.
  47. Himeidan YE, Kweka EJ, , 2012. Malaria in east African highlands during the past 30 years: impact of environmental changes. Front Physiol 3: 315.[Crossref]
  48. Hay SI, Shanks GD, Stern DI, Snow RW, Randolph SE, Rogers DJ, , 2005. Climate variability and malaria epidemics in the highlands of east Africa. Trends Parasitol 21: 5253.[Crossref]
  49. Hales S, Woodward A, , 2005. Global climate change and malaria. Lancet Infect Dis 5: 258259.[Crossref]
  50. Thomas CJ, Davies G, Dunn CE, , 2004. Mixed picture for changes in stable malaria distribution with future climate in Africa. Trends Parasitol 20: 216220.[Crossref]
  51. Chaves LF, Koenraadt CJM, , 2010. Climate change and highland malaria: fresh air for a hot debate. Q Rev Biol 85: 2755.[Crossref]
  52. Abeku TA, Kristan M, Jones C, Beard J, Mueller DH, Okia M, Rapuoda B, Greenwood B, Cox J, , 2008. Determinants of the accuracy of rapid diagnostic tests in malaria case management: evidence from low and moderate transmission settings in the east African highlands. Malar J 7: 202.[Crossref]
  53. Ghebreyesus TA, Haile M, Witten KH, Getachew A, Yohannes AM, Yohannes M, Teklehaimanot HD, Lindsay SW, Byass P, , 1999. Incidence of malaria among children living near dams in northern Ethiopia: community based incidence survey. BMJ 319: 663666.[Crossref]
  54. Garnham PCC, , 1945. Malaria epidemics at exceptionally high altitudes in Kenya. BMJ 2: 4547.[Crossref]
  55. Lynch C, Roper C, , 2011. The transit phase of migration: circulation of malaria and its multidrug-resistant forms in Africa. PLoS Med 8: e1001040.[Crossref]
  56. Anderson TJC, Roper C, , 2005. The origins and spread of antimalarial drug resistance: lessons for policy makers. Acta Trop 94: 269280.[Crossref]
  57. Lynch C, Pearce R, Pota H, Cox J, Abeku TA, Rwakimari J, Naidoo I, Tibenderana J, Roper C, , 2008. Emergence of a dhfr mutation conferring high-level drug resistance in Plasmodium falciparum populations from southwest Uganda. J Infect Dis 197: 15981604.[Crossref]
  58. Alifrangis M, Nag S, Schousboe ML, Ishengoma D, Lusingu J, Pota H, Kavishe RA, Pearce R, Ord R, Lynch C, Dejene S, Cox J, Rwakimari J, Minja DTR, Lemnge MM, Roper C, , 2014. Independent origin of Plasmodium falciparum antifolate super-resistance, Uganda, Tanzania, and Ethiopia. Emerg Infect Dis 20: 12801286.[Crossref]
  59. Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot OJ, Moonen B, , 2012. Malaria resurgence: a systematic review and assessment of its causes. Malar J 11: 122.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.15-0653
Loading
/content/journals/10.4269/ajtmh.15-0653
Loading

Data & Media loading...

Supplementary Data

Supplementary PDF

  • Received : 09 Sep 2015
  • Accepted : 03 Mar 2016

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error