Changing patterns of malaria epidemiology between 2002 and 2010 in Western Kenya: the fall and rise of malaria

Guofa Zhou, Yaw A Afrane, Anne M Vardo-Zalik, Harrysone Atieli, Daibin Zhong, Peter Wamae, Yousif E Himeidan, Noboru Minakawa, Andrew K Githeko, Guiyun Yan, Guofa Zhou, Yaw A Afrane, Anne M Vardo-Zalik, Harrysone Atieli, Daibin Zhong, Peter Wamae, Yousif E Himeidan, Noboru Minakawa, Andrew K Githeko, Guiyun Yan

Abstract

Background: The impact of insecticide treated nets (ITNs) on reducing malaria incidence is shown mainly through data collection from health facilities. Routine evaluation of long-term epidemiological and entomological dynamics is currently unavailable. In Kenya, new policies supporting the provision of free ITNs were implemented nationwide in June 2006. To evaluate the impacts of ITNs on malaria transmission, we conducted monthly surveys in three sentinel sites with different transmission intensities in western Kenya from 2002 to 2010.

Methods and findings: Longitudinal samplings of malaria parasite prevalence in asymptomatic school children and vector abundance in randomly selected houses were undertaken monthly from February 2002. ITN ownership and usage surveys were conducted annually from 2004 to 2010. Asymptomatic malaria parasite prevalence and vector abundances gradually decreased in all three sites from 2002 to 2006, and parasite prevalence reached its lowest level from late 2006 to early 2007. The abundance of the major malaria vectors, Anopheles funestus and An. gambiae, increased about 5-10 folds in all study sites after 2007. However, the resurgence of vectors was highly variable between sites and species. By 2010, asymptomatic parasite prevalence in Kombewa had resurged to levels recorded in 2004/2005, but the resurgence was smaller in magnitude in the other sites. Household ITN ownership was at 50-70% in 2009, but the functional and effective bed net coverage in the population was estimated at 40.3%, 49.4% and 28.2% in 2010 in Iguhu, Kombewa, and Marani, respectively.

Conclusion: The resurgence in parasite prevalence and malaria vectors has been observed in two out of three sentinel sites in western Kenya despite a high ownership of ITNs. The likely factors contributing to malaria resurgence include reduced efficacy of ITNs, insecticide resistance in mosquitoes and lack of proper use of ITNs. These factors should be targeted to avoid further resurgence of malaria transmission.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Dynamics of Plasmodium falciparum parasite…
Figure 1. Dynamics of Plasmodium falciparum parasite prevalence (%) from 2002 to 2010.
Study site from top to bottom: Kombewa, Iguhu, and Marani. The timings of major changes in ITN/LLIN distribution policy were marked on top.
Figure 2. Dynamics of Plasmodium falciparum infection…
Figure 2. Dynamics of Plasmodium falciparum infection intensity and gametocyte prevalence (%) from 2002 to 2010.
Study site from top to bottom: Kombewa, Iguhu, and Marani.
Figure 3. Temporal dynamics of Anopheles gambiae…
Figure 3. Temporal dynamics of Anopheles gambiae s.l. (left panel) and An. funestus (right panel) density (number of females/house/night) from 2002 to 2010.
Figure 4. Species composition of Anopheles gambiae…
Figure 4. Species composition of Anopheles gambiae s.s. and An. arabiensis in Kombewa (top) and Iguhu (bottom) from 2003 to 2010.
Figure 5. A) Increase in bed net…
Figure 5. A) Increase in bed net ownership, presented as the percentage of households owning at least one net, from 2004 to 2010 (top); B) percentage of bed net coverage among the population in 2010 (bottom).
Effective bed net coverage is defined as the proportion of the population who slept under LLINs in good condition, or slept under regular ITNs in good condition and that were routinely insecticide-retreated. Ineffective population coverage by bed net is defined as the proportion of the population who slept under torn nets, or slept under regular ITNs but not routinely insecticide-retreated.
Figure 6. Variations in monthly maximum temperature,…
Figure 6. Variations in monthly maximum temperature, minimum temperature, mean temperature and monthly rainfalls in Kombewa (top), Iguhu (middle) and Marani (bottom) from 2002 to 2010.

References

    1. World Health Organization. Geneva 2008: WHO; 2008. World Malaria Report 2008.
    1. Ceesay SJ, Casals-Pascual C, Erskine J, Anya SE, Duah NO, et al. Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet. 2008;372:1523–1525.
    1. Bhattarai A, Ali AS, Kachur SP, Mårtensson A, Abbas AK, et al. Impact of artemisinin-based combination therapy and insecticide-treated nets on malaria burden in Zanzibar. PLoS Med. 2007;4:e309.
    1. World Health Organization. Geneva: Switzerland; 2009. World Malaria Report 2009.
    1. Otten M, Aregawi M, Were W, Karema C, Medin A, et al. Initial evidence of reduction of malaria cases and deaths in Rwanda and Ethiopia due to rapid scale-up of malaria prevention and treatment. Malaria J. 2009;8:14.
    1. Hsiang MS, Abeyasinghe R, Whittaker M, Feachem RGA. Malaria elimination in Asia-Pacific: an under-told story. Lancet. 2010;375:1586–1587.
    1. World Health Organization. Geneva: Switzerland; 2008. Global malaria control and elimination: report of a technical review.
    1. Roll Back Malaria. Geneva: Switzerland; 2009. Malaria Elimination in Africa. WHO RBM/EXD/2009/STATE.2.
    1. Slutsker L, Newman RD. Malaria scale-up progress: is the glass half-empty or half-full? Lancet. 2009;373:11–13.
    1. Müller O, Yé M, Louis VR, Sié A. Malaria in sub-Saharan Africa. Lancet. 2009;373:122.
    1. Knols BGJ. Malaria elimination: When the tools are great but implementation falters. Am J Trop Med Hyg. 2010;82:174–175.
    1. Fegan GW, Noor AM, Akhwale WS, Cousens S, Snow RW. Effect of expanded insecticide-treated bed net coverage on child survival in rural Kenya: a longitudinal study. Lancet. 2007;370:1035–1039.
    1. Okech BA, Mwobobia IK, Kamau A, Muiruri S, Mutiso N, et al. Use of integrated malaria management reduces malaria in Kenya. PLoS ONE. 2008;3:e4050.
    1. Okiro EA, Hay SI, Gikandi PW, Sharif SK, Noor AM, et al. The decline in paediatric malaria admissions on the coast of Kenya. Malaria J. 2007;6:151.
    1. O'Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, et al. Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet. 2008;372:1555–1562.
    1. Lengeler C, deSavigny D. Programme diversity is key to the success of insecticide-treated bed nets. Lancet. 2007;370:1009–1010.
    1. Okiro EA, Alegana VA, Noor AM, Mutheu JJ, Juma E, et al. Malaria paediatric hospitalization between 1999 and 2008 across Kenya. BMC Med. 2009;7:75.
    1. Okiro EA, Alegana VA, Noor AM, Snow RW. Changing malaria intervention coverage, transmission and hospitalization in Kenya. Malaria J. 2010;9:285.
    1. Zurovac D, Njogu J, Akhwale W, Hamer DH, Larson AB, et al. Effects of revised diagnostic recommendations on malaria treatment practices across age groups in Kenya. Trop Med Int Health. 2008;13:784–787.
    1. Noor AM, Amin AA, Akhwale WS, Snow RW. Increasing coverage and decreasing inequity in insecticide-treated bed net use among rural Kenyan children. PLoS Med. 2007;4:e255.
    1. Guerra CA, Gikandi PW, Tatem AJ, Noor AM, Smith DL, et al. The limits and intensity of Plasmodium falciparum transmission: implications for malaria control and elimination worldwide. PLoS Med. 2008;5:e38.
    1. Lindblade KA, Eisele TP, Gimnig JE, Alaii JA, Odhiambo F, et al. Sustainability of reductions in malaria transmission and infant mortality in western Kenya with use of insecticide-treated bednets: 4 to 6 years of follow up. JAMA. 2004;291:2571–2580.
    1. Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, et al. Impact of sustained use of insecticide-treated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol. 2006;43:428–432.
    1. Afrane YA, Githeko AK, Yan G. Misdiagnosis and overtreatment of clinical malaria cases and their implications in Western Kenya highlands. Am J Trop Med Hyg. 2009;81(Suppl):195.
    1. Rowe AK, Kachur PS, Yoon SS, Lynch M, Slutsker L, et al. Caution is required when using health facility-based data to evaluate the health impact of malaria control efforts in Africa. Malaria J. 2009;8:209.
    1. World Health Organization. Geneva: WHO; 2005. Insecticide-treated mosquito nets: a WHO position statement. . Accessed Dec 20, 2010.
    1. Munyekenye OG, Githeko AK, Zhou G, Mushinzimana E, Minakawa N, et al. Plasmodium falciparum spatial analysis, western Kenya highlands. Emerg Infect Dis. 2005;11:1571–1577.
    1. Minakawa N, Sonye G, Mogi M, Githeko AK, Yan G. The effects of climatic factors on the distribution and abundance of malaria vectors in Kenya. J Med Entomol. 2002;39:833–841.
    1. Ndenga B, Githeko AK, Omukunda E, Munyekenye OG, Atieli H, et al. Population dynamics of malaria vectors in western Kenya highlands. J Med Entomol. 2006;43:200–206.
    1. World Health Organization. Methods and techniques. Geneva: WHO; 1975. Manual on practical entomology in malaria, Part II. No13.
    1. Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa South of the Sahara (Afrotropical Region). Johannesburg, South Africa Institute for Medical Research, No 55. 1987.
    1. World Health Organization. Geneva: World Health Organization; 2005. Guidelines for laboratory and field testing of longlasting insecticidal mosquito nets. WHO/CDS/WHOPES/GCDPP/2005.11, . Accessed Dec 20, 2010.
    1. Kamau L, Agai D, Matoke D, Wachira L, Gikandi G, et al. Status of Insecticide Susceptibility in Anopheles gambiae Sensu Lato and Anopheles funestus Mosquitoes from Western Kenya. J Insect Sci. 2008;8:1–7.
    1. Erlanger TE, Enayati AA, Hemingway J, Mshinda H, Tami A, et al. Field issues related to effectiveness of insecticide-treated nets in Tanzania. Med Vet Entomol. 2004;18:153–160.
    1. Maxwell CA, Rwegoshora T, Magesa SM, Curtis CF. Comparison of coverage with insecticide-treated nets in a Tanzanian town and villages where nets and insecticide are either marketed or provided free of charge. Malar J. 2006;5:44.
    1. Hamilton JD. Princeton University Press; 1994. Time Series Analysis.799
    1. Bayoh NM, Mathias DK, Odiere MR, Mutuku FM, Kamau L, et al. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya. Malaria J. 2010;9:62.
    1. Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, et al. Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Am J Trop Med Hyg. 2003;68(Suppl 4):16–22.
    1. Das P, Horton R. Malaria elimination: worthy, challenging, and just possible. Lancet. 2010;376:1515–1517.
    1. Flaxman AD, Fullman N, Otten MW, Menon M, Cibulskis RE, et al. Rapid scaling up of insecticide-treated bed net coverage in Africa and its relationship with development assistance for health: A systematic synthesis of supply, distribution, and household survey data. PLoS Med. 2010;7:e1000328. doi: .
    1. Eisele TP, Keating J, Littrell M, Larsen D, Macintyre K. Assessment of insecticide-treated bednet use among children and pregnant women across 15 countries using standardized national surveys. Am J Trop Med Hyg. 2009;80:209–214.
    1. N'Guessan R, Darriet F, Doannio, Chandre P, Carnevale P. Olyset Net® efficacy against pyrethroid-resistant Anopheles gambiae and Culex quinquefasciatus after 3 years' field use in Côte d'Ivoire. Med Vet Entomol. 2001;15:97–104.
    1. World Health Organization. Geneva: WHO; 2009. Report of the thirteenth WHOPES working group meeting: review of Olyset LN, Dawaplus 2.0 LN, Tianjin Yorkool LN. WHO/HTM/NTD/WHOPES/2009.5.
    1. Chen H, Githeko AK, Kithure JI, Mutunga J, Zhou G, et al. Monooxygenase levels and knockdown resistance (kdr) allele frequencies in Anopheles gambiae and Anopheles arabiensis in Kenya. J Med Entomol. 2008;45:242–250.
    1. Githeko AK, Adungo NI, Karanja DM, Hawley WA, Vulule JM, et al. Some observations on the biting behavior of Anopheles gambiae s.s., Anopheles arabiensis, and Anopheles funestus and their implications for malaria control. Exp Parasitol. 1996;82:306–315.
    1. Mathenge EM, Gimnig JE, Kolczak M, Ombok M, Irungu LW, et al. Effect of permethrin-impregnated nets on exiting behavior, blood feeding success, and time of feeding of malaria mosquitoes (Diptera: Culicidae) in western Kenya. J Med Entomol. 2001;38:531–536.
    1. Govella NJ, Okumu FO, Killeen GF. Insecticide-treated nets can reduce malaria transmission by mosquitoes which feed outdoors. Am J Trop Med Hyg. 2010;82:415–419.
    1. Mathias DK, Ochomo E, Atieli F, Ombok M, Bayoh NM, et al. Spatial and temporal variation in the kdr allele L1014S in Anopheles gambiae s.s. and phenotypic variability in susceptibility to insecticides in Western Kenya. Malaria J. 2011;10:10.
    1. Brooker S, Kolaczinski JH, Gitonga CW, Noor AM, Snow RW. The use of schools for malaria surveillance and programme evaluation in Africa. Malaria J. 2009;8:231.
    1. Noor AM, Kirui VC, Brooker SJ, Snow RW. The use of insecticide treated nets by age: implications for universal coverage in Africa. BMC Public Health. 2009;9:369.
    1. Githinji S, Herbst S, Kistemann T, Noor AM. Mosquito nets in a rural area of Western Kenya: ownership, use and quality. Malaria J. 2010;9:250.
    1. The Lancet. Maintaining momentum for malaria elimination. Lancet. 2009;374:266.
    1. Whitty CJM, Chandler C, Ansah E, Leslie T, Staedke SG. Deployment of ACT antimalarials for treatment of malaria: challenges and opportunities. Malaria J. 2008;7(Suppl 1):S7.
    1. Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, et al. Ecology: a prerequisite for malaria elimination and eradication. PLoS Med. 2010;7:e1000303. doi: .
    1. Chaves LF, Kaneko A, Taleo G, Pascual M, Wilson ML. Malaria transmission pattern resilience to climatic variability is mediated by insecticide-treated nets. Malaria J. 2008;7:100.
    1. Shah NK. Assessing strategy and equity in the elimination of malaria. PLoS Med. 2010;7:e1000312. doi: .
    1. Kouyaté B, Sie A, Ye M, Allegri MD, Muller O. The great failure of malaria control in Africa: a district perspective from Burkina Faso. PLoS Med. 2007;4:e127.
    1. Beier JC, Keating J, Githure JI, Macdonald MB, Impoinvil DE, et al. Integrated vector management for malaria control. Malaria J. 2008;7(Suppl 1):S4.
    1. Takken W, Knols BGJ. Malaria vector control: current and future strategies. Trends Parasitol. 2009;25:101–104.
    1. Greenwood B. Can malaria be eliminated? Trans R Soc Trop Med Hyg. 2009;103(suppl):2–5.

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