Serological markers for monitoring historical changes in malaria transmission intensity in a highly endemic region of Western Kenya, 1994-2009

Malaria Journal

Volumn 13, Issue 1, 2014, Pages

  Wong, Jacklyn ^a   Hamel, Mary J ^a   Drakeley, Chris J ^b   Kariuki, Simon ^c   Shi, Ya Ping ^a   Lal, Altaf A ^a   Nahlen, Bernard L ^a   Bloland, Peter B ^a   Lindblade, Kim A ^a   Were, Vincent ^c   Otieno, Kephas ^c   Otieno, Peter ^c   Odero, Chris ^c   Slutsker, Laurence ^a   Vulule, John M ^c   Gimnig, John E ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^c KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

Author keywords

Antibodies; Epidemiology; Malaria; Plasmodium falciparum; Serology; Transmission intensity

Indexed keywords

ADOLESCENT; ADULT; AGE DISTRIBUTION; AGED; ANALYTICAL PARAMETERS; ANTIBODY TITER; CHILD; DISEASE MARKER; ENDEMIC DISEASE; ENTOMOLOGICAL INOCULATION RATE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENERAL ASPECTS OF DISEASE; HISTORY OF MEDICINE; HUMAN; IMMUNOGENICITY; INFECTION RISK; INSECTICIDE TREATED NET; KENYA; MAJOR CLINICAL STUDY; MALARIA; MALARIA TRANSMISSION INTENSITY; MALE; MIDDLE AGED; MONITORING; PARASITE PREVALENCE; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; PROGRAMMATIC MONITORING; RETROSPECTIVE STUDY; REVIEW; SEROCONVERSION RATE; SEROLOGY; SEROPREVALENCE; TIME SERIES ANALYSIS; TREND STUDY; VERY ELDERLY; YOUNG ADULT; BLOOD; IMMUNOLOGY; INFANT; MALARIA, FALCIPARUM; TRANSMISSION;

APICAL MEMBRANE ANTIGEN I, PLASMODIUM; CIRCUMSPOROZOITE PROTEIN, PROTOZOAN; MEMBRANE PROTEIN; MEROZOITE SURFACE PROTEIN 1; PARASITE ANTIGEN; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CHILD; CHILD, PRESCHOOL; HUMANS; INFANT; KENYA; MALARIA, FALCIPARUM; MALE; MEMBRANE PROTEINS; MEROZOITE SURFACE PROTEIN 1; MIDDLE AGED; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RETROSPECTIVE STUDIES; SEROEPIDEMIOLOGIC STUDIES; YOUNG ADULT;

EID: 84964315661     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-13-451     Document Type: Review

References (61)

1. Smith DL, Dushoff J, Snow RW, Hay SI: The entomological inoculation rate and Plasmodium falciparum infection in African children. Nature 2005, 438:492-495.
2. Hay SI, Smith DL, Snow RW: Measuring malaria endemicity from intense to interrupted transmission. Lancet Infect Dis 2008, 8:369-378.
3. Kelly-Hope LA, McKenzie FE: The multiplicity of malaria transmission: a review of entomological inoculation rate measurements and methods across sub-Saharan Africa. Malar J 2009, 8:19.
4. Byass P: Making sense of long-term changes in malaria. Lancet 2008, 372:1523-1525.
5. Breman JG: The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am J Trop Med Hyg 2001, 64:1-11.
6. Rowe AK, Kachur SP, Yoon SS, Lynch M, Slutsker L, Steketee RW: Caution is required when using health facility-based data to evaluate the health impact of malaria control efforts in Africa. Malar J 2009, 8:3.
7. Afrane YA, Githeko A, Yan GY: Misdiagnosis and overtreatment of clinical malaria cases and their implications in western Kenya highlands. Am J Trop Med Hyg 2009, 81:195-195.
8. Beier JC, Killeen GF, Githure JI: Short report: entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. Am J Trop Med Hyg 1999, 61:109-113.
9. Hay SI, Rogers DJ, Toomer JF, Snow RW: Annual Plasmodium falciparum entomological inoculation rates (EIR) across Africa: literature survey, internet access and review. Trans R Soc Trop Med Hyg 2000, 94:113-127.
10. Dye C: The analysis of parasite transmission by bloodsucking insects. Ann Rev Entomol 1992, 37:1-19.
11. Mbogo CN, Glass GE, Forster D, Kabiru EW, Githure JI, Ouma JH, Beier JC: Evaluation of light traps for sampling Anopheline mosquitoes in Kilifi, Kenya. J Am Mosquito Contr 1993, 9:260-263.
12. Magbity EB, Lines JD: Spatial and temporal distribution of Anopheles gambiae s.l. (Diptera: Culicidae) in two Tanzanian villages: implication for designing mosquito sampling routines. Bull Entomol Res 2002, 92:483-488.
13. Tusting LS, Bousema T, Smith DL, Drakeley C: Measuring changes in Plasmodium falciparum transmission: precision, accuracy and costs of metrics. In Advances in Parasitology. Volume 84. Edited by Rollinson D. San Diego: Elsevier Academic Press Inc; 2014:151-208.
14. Smith DL, Drakeley CJ, Chiyaka C, Hay SI: A quantitative analysis of transmission efficiency versus intensity for malaria. Nat Comm 2010, 1:108. doi:10.1038/ncomms1107.
15. Yukich J, Briët O, Bretscher MT, Bennett A, Lemma S, Berhane Y, Eisele TP, Keating J, Smith T: Estimating Plasmodium falciparum transmission rates in low-endemic settings using a combination of community prevalence and health facility data. PLoS One 2012, 7:e42861.
16. Corran P, Coleman P, Riley E, Drakeley C: Serology: a robust indicator of malaria transmission intensity? Trends Parasitol 2007, 23:575-582.
17. O'Meara WP, Collins WE, McKenzie FE: Parasite prevalence: a static measure of dynamic infections. Am J Trop Med Hyg 2007, 77:246-249.
18. Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SLR, Carneiro I, Malima R, Lusingu J, Manjurano A, Nkya WMM, Lemnge MM, Cox J, Reyburn H, Riley EM: Estimating medium-and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci U S A 2005, 102:5108-5113.
19. Bousema T, Youssef RM, Cook J, Cox J, Alegana VA, Amran J, Noor AM, Snow RW, Drakeley C: Serologic markers for detecting malaria in areas of low endemicity, Somalia, 2008. Emerg Infect Dis 2010, 16:392-399.
20. Cornille-Brogger R, Mathews HM, Storey J, Ashkar TS, Brogger S, Molineaux L: Changing patterns in the humoral immune response to malaria before, during, and after the application of control measures: a longitudinal study in the West African savanna. Bull World Health Organ 1978, 56:579-600.
21. Stewart L, Gosling R, Griffin J, Gesase S, Campo J, Hashim R, Masika P, Mosha J, Bousema T, Shekalaghe S, Cook J, Corran P, Ghani A, Riley EM, Drakeley C: Rapid assessment of malaria transmission using age-specific sero-conversion rates. PLoS One 2009, 4:e6083.
22. Cook J, Kleinschmidt I, Schwabe C, Nseng G, Bousema T, Corran PH, Riley EM, Drakeley CJ: Serological markers suggest heterogeneity of effectiveness of malaria control interventions on Bioko Island. Equatorial Guinea PLoS One 2011, 6:e25137.
23. Lim CS, Yoon JK, Chang EA, Suh IB, An SSA, Lee KH, Chung JT, Tockgo YC: Seroprevalence to the circumsporozoite protein peptide antigen of Plasmodium vivax in Korean children. Microbiol Immunol 2005, 49:521-527.
24. Cook J, Reid H, Iavro J, Kuwahata M, Taleo G, Clements A, McCarthy J, Vallely A, Drakeley C: Using serological measures to monitor changes in malaria transmission in Vanuatu. Malar J 2010, 9:169.
25. Druilhe P, Pradier O, Marc JP, Miltgen F, Mazier D, Parent G: Levels of antibodies to Plasmodium falciparum sporozoite surface antigens reflect malaria transmission rates and are persistent in the absence of reinfection. Infect Immun 1986, 53:393-397.
26. Hsiang MS, Hwang J, Kunene S, Drakeley C, Kandula D, Novotny J, Parizo J, Jensen T, Tong M, Kemere J, Dlamini S, Moonen B, Angov E, Dutta S, Ockenhouse C, Dorsey D, Greenhouse B: Surveillance for malaria elimination in Swaziland: a national cross-sectional study using pooled PCR and serology. PLoS One 2012, 7:e29550.
27. Bloland PB, Ruebush TK, McCormick JB, Ayisi J, Boriga DA, Oloo AJ, Beach R, Hawley W, Lal A, Nahlen B, Udhayakumar V, Campbell CC: Longitudinal cohort study of the epidemiology of malaria infections in an area of intense malaria transmission I. Description of study site, general methodology, and study population. Am J Trop Med Hyg 1999, 60:635-640.
28. Phillips-Howard PA, Nahlen BL, Alaii JA, ter Kuile FO, Gimnig JE, Terlouw DJ, Kachur SP, Hightower AW, Lal AA, Schoute E, Oloo AJ, Hawley WA: The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya I. Development of infrastructure and description of study site. Am J Trop Med Hyg 2003, 68:3-9.
29. Phillips-Howard PA, ter Kuile FO, Nahlen BL, Alaii JA, Gimnig JE, Kolczak MS, Terlouw DJ, Kariuki SK, Shi YP, Kachur SP, Hightower AW, Vulule JM, Hawley WA: The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya II. Study design and methods. Am J Trop Med Hyg 2003, 68:10-15.
30. Lindblade KA, Eisele TP, Gimnig JE, Alaii JA, Odhiambo F, ter Kuile FO, Hawley WA, Wannemuehler KA, Phillips-Howard PA, Rosen DH, Nahlen BL, Terlouw DJ, Adazu K, Vulule JM, Slutsker L: 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. J Am Med Assoc 2004, 291:2571-2580.
31. Hamel MJ, Adazu K, Obor D, Sewe M, Vulule J, Williamson JM, Slutsker L, Feikin DR, Laserson KF: A reversal in reductions of child mortality in western Kenya, 2003-2009. Am J Trop Med Hyg 2011, 85:597-605.
32. Singer LM, Mirel LB, Kuile FO, Branch OH, Vulule JM, Kolczak MS, Hawley WA, Simon KK, Kaslow DC, Lanar DE, Lai AA: The effects of varying exposure to malaria transmission on development of antimalarial antibody responses in preschool children. XVI. Asembo Bay cohort project. J Infect Dis 2003, 187:1756-1764.
33. Webster HK, Gingrich JB, Wongsrichanalai C, Tulyayon S, Suvarnamani A, Sookto P, Permpanich B: Circumsporozoite antibody as a serologic marker of Plasmodium falciparum transmission. Am J Trop Med Hyg 1992, 47:489-497.
34. Esposito F, Lombardi S, Modiano D, Zavala F, Reeme J, Lamizana L, Coluzzi M, Nussenzweig RS: Prevalence and levels of antibodies to the circumsporozoite protein of Plasmodium falciparum in an endemic area an their relationship to resistance against malaria infection. Trans R Soc Trop Med Hyg 1988, 82:827-832.
35. Badu K, Afrane YA, Larbi J, Stewart VA, Waitumbi J, Angov E, Ong'echa JM, Perkins DJ, Zhou G, Githeko A, Yan G: Marked variation in MSP-1(19) antibody responses to malaria in western Kenyan highlands. BMC Infect Dis 2012, 12:50.
36. Bloland PB, Boriga DA, Ruebush TK, McCormick JB, Roberts JM, Oloo AJ, Hawley W, Lal A, Nahlen B, Campbell CC: Longitudinal cohort study of the epidemiology of malaria infections in an area of intense malaria transmission II. Descriptive epidemiology of malaria infection and disease among children. Am J Trop Med Hyg 1999, 60:641-648.
37. Beier JC, Perkins PV, Onyango FK, Gargan TP, Oster CN, Whitmire RE, Koech DK, Roberts CR: Characterization of malaria transmission by Anopheles (Diptera, Culicidae) in western Kenya in preparation for malaria vaccine trials. J Med Entomol 1990, 27:570-577.
38. Beier JC, Oster CN, Onyango FK, Bales JD, Sherwood JA, Perkins PV, Chumo DK, Koech DV, Whitmire RE, Roberts CR, Diggs CL, Hoffman SL: Plasmodium falciparum incidence relative to entomological inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Am J Trop Med Hyg 1994, 50:529-536.
39. ter Kuile FO, Terlouw DJ, Phillips-Howard PA, Hawley WA, Friedman JF, Kolczak MS, Kariuki SK, Shi YP, Kwena AM, Vulule JM, Nahlen BL: Impact of permethrin-treated bed nets on malaria and all-cause morbidity in young children in an area of intense perennial malaria transmission in western Kenya: cross-sectional survey. Am J Trop Med Hyg 2003, 68:100-107.
40. Gimnig JE, Vulule JM, Lo TQ, Kamau L, Kolczak MS, Phillips-Howard PA, Mathenge EM, ter Kuile FO, Nahlen BL, Hightower AW, Hawley WA: Impact of permethrin-treated bed nets on entomologic indices in an area of intense year-round malaria transmission. Am J Trop Med Hyg 2003, 68:16-22.
41. Lindblade KA, Gimnig JE, Kamau L, Hawley WA, Odhiambo F, Olang G, Ter Kuile FO, Vulule JM, Slutsker L: Impact of sustained use of insecticidetreated bednets on malaria vector species distribution and culicine mosquitoes. J Med Entomol 2006, 43:428-432.
42. Amek N, Bayoh N, Hamel M, Lindblade KA, Gimnig JE, Odhiambo F, Laserson KF, Slutsker L, Smith T, Vounatsou P: Spatial and temporal dynamics of malaria transmission in rural Western Kenya. Parasit Vectors 2012, 5:86.
43. Adazu K, Lindblade KA, Rosen DH, Odhiambo F, Ofware P, Kwach J, van Eijk AM, Decock KM, Amornkul P, Karanja D, Vulule JM, Slutsker L: Health and demographic surveillance in rural western Kenya: a platform for evaluating interventions to reduce morbidity and mortality from infectious diseases. Am J Trop Med Hyg 2005, 73:1151-1158.
44. Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I, Esser KM, Beaudoin RL, Andre RG: Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ 1987, 65:39-45.
45. Scott JA, Brogdon WG, Collins FH: Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 1993, 49:520-529.
46. Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, Griffin J, Cox J, Abeku T, Bousema T, Ghani AC, Drakeley C, Riley EM: Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malar J 2008, 7:195.
47. Odhiambo FO, Laserson KF, Sewe M, Hamel MJ, Feikin DR, Adazu K, Ogwang S, Obor D, Amek N, Bayoh N, Ombok M, Lindblade K, Desai M, ter Kuile F, Phillips-Howard P, van Eijk AM, Rosen D, Hightower A, Ofware P, Muttai H, Nahlen B, DeCock K, Slutsker L, Beriman R, Vulule JM: Profile: the KEMRI/CDC Health and Demographic Surveillance System-Western Kenya. Int J Epidemiol 2012, 41:977-987.
48. Ondigo BN, Hodges JS, Ireland KF, Magak NG, Lanar DE, Dutta S, Narum DL, Park GS, Ofulla AV, John CC: Estimation of recent and long-term malaria transmission in a population by antibody testing to multiple Plasmodium falciparum antigens. J Infect Dis 2014, 210:1123-1132.
49. Reed GF, Meade BD, Steinhoff MC: The reverse cumulative distribution plot-a graphic method for exploratory analysis of antibody data. Pediatrics 1995, 96:600-603.
50. Deloron P, Steketee R, Campbell GH, Peyron F, Kaseje D, Brandling-Bennett AD: Serological reactivity to the ring-infected erythrocyte surface antigen and circumsporozoite protein in gravid and nulligravid women infected with Plasmodium falciparum. Trans R Soc Trop Med Hyg 1989, 83:58-62.
51. Campbell CC, Martinez JM, Collins WE: Seroepidemiological studies of malaria in pregnant women and newborns from coastal El Salvador. Am J Trop Med Hyg 1980, 29:151-157.
52. Kariuki SK, Lal AA, Terlouw DJ, ter Kuile FO, Ong'echa JM, Phillips-Howard PA, Orago ASS, Kolczak MS, Hawley WA, Nahlen BL, Shi YP: Effects of permethrin-treated bed nets on immunity to malaria in western Kenya II. Antibody responses in young children in an area of intense malaria transmission. Am J Trop Med Hyg 2003, 68:108-114.
53. Phillips-Howard PA, Nahlen BL, Kolczak MS, Hightower AW, ter Kuile FO, Alaii JA, Gimnig JE, Arudo J, Vulule JM, Odhacha A, Kachur SP, Schoute E, Rosen DH, Sexton JD, Oloo AJ, Hawley WA: Efficacy of permethrin-treated bed nets in the prevention of mortality in young children in an area of high perennial malaria transmission in western Kenya. Am J Trop Med Hyg 2003, 68:23-29.
54. Perkins BA, Zucker JR, Otieno J, Jafari HS, Paxton L, Redd SC, Nahlen BL, Schwartz B, Oloo AJ, Olango C, Gove S, Campbell CC: Evaluation of an algorithm for integrated management of childhood illness in an area of Kenya with high malaria transmission. Bull World Health Organ 1997, 75(Suppl 1):33-42.
55. Pindolia DK, Garcia AJ, Huang Z, Smith DL, Alegana VA, Noor AM, Snow RW, Tatem AJ: The demographics of human and malaria movement and migration patterns in East Africa. Malar J 2013, 12:12.
56. Wesolowski A, Eagle N, Tatem AJ, Smith DL, Noor AM, Snow RW, Buckee CO: Quantifying the impact of human mobility on malaria. Science 2012, 338:267-270.
57. Davis JR, Hall T, Chee EM, Majala A, Minjas J, Shiff CJ: Comparison of sampling anopheline mosquitoes by light-trap and human-bait collections indoors at Bagamoyo, Tanzania. Med Vet Entomol 1995, 9:249-255.
58. Mathenge EM, Omweri GO, Irungu LW, Ndegwa PN, Walczak E, Smith TA, Killeen GF, Knols BGJ: Comparative field evaluation of the Mbita trap, the Centers for Disease Control light trap, and the human landing catch for sampling of malaria vectors in western Kenya. Am J Trop Med Hyg 2004, 70:33-37.
59. Bosomprah S: A mathematical model of seropositivity to malaria antigen, allowing seropositivity to be prolonged by exposure. Malar J 2014, 13:12.
60. Drakeley C, Cook J: Potential contribution of sero-epidemiological analysis for monitoring malaria control and elimination: historical and current perspectives. In Adv Parasitol 2009, 69:299-352.
61. Akpogheneta OJ, Duah NO, Tetteh KKA, Dunyo S, Lanar DE, Pinder M, Conway DJ: Duration of naturally acquired antibody responses to blood-stage Plasmodium falciparum is age dependent and antigen specific. Infect Immun 2008, 76:1748-1755.