The silent threat: Asymptomatic parasitemia and malaria transmission

Expert Review of Anti-Infective Therapy

Volumn 11, Issue 6, 2013, Pages 623-639

  Lindblade, Kim A ^a   Steinhardt, Laura ^a   Samuels, Aaron ^a   Kachur, S Patrick ^a   Slutsker, Laurence ^a  

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

Author keywords

antimalarial; asymptomatic; elimination; infection; interventions; malaria; parasite

Indexed keywords

ANTIMALARIAL AGENT; ARTESUNATE; CHLOROQUINE; DIHYDROARTEMISININ PLUS PIPERAQUINE; PRIMAQUINE; PYRIMETHAMINE PLUS SULFADOXINE;

ASYMPTOMATIC INFECTION; DRUG USE; ENDEMIC DISEASE; HUMAN; LOW DRUG DOSE; MALARIA; MALARIA CONTROL; MORBIDITY; MORTALITY; MOSQUITO; PARASITE VECTOR; PARASITEMIA; PATHOGEN CLEARANCE; REVIEW;

ADOLESCENT; ADULT; AGED; ANIMALS; ANOPHELES GAMBIAE; ASYMPTOMATIC INFECTIONS; CHILD; CHILD, PRESCHOOL; DISEASE VECTORS; HUMANS; INFANT; INFANT, NEWBORN; MALARIA, FALCIPARUM; MIDDLE AGED; PARASITEMIA; PLASMODIUM FALCIPARUM;

EID: 84878840749     PISSN: 14787210     EISSN: 17448336     Source Type: Journal    
DOI: 10.1586/eri.13.45     Document Type: Review

References (132)

1. WHO. World Malaria Report 2011. WHO, Geneva, Switzerland (2011).
2. African Union. Fight Malaria: Africa Goes from Control to Elimination by 2010. African Union, Johannesburg, South Africa (2007).
3. Feachem R, Sabot O. A new global malaria eradication strategy. Lancet 371(9624), 1633-1635 (2008).
4. UCSF Global Health Group; Malaria Atlas Project.Atlas of Malaria-Eliminating Countries, 2011. The Global Health Group, CA, USA (2011).
5. Hamel MJ, Adazu K, Obor D et al. A reversal in reductions of child mortality in western Kenya, 2003-2009. Am. J. Trop. Med. Hyg. 85(4), 597-605 (2011).
6. Bloland PB, Ruebush TK, McCormick JB et al. 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. 60(4), 635-640 (1999).
7. Eisele TP, Miller JM, Moonga HB, Hamainza B, Hutchinson P, Keating J. Malaria infection and anemia prevalence in Zambia's Luangwa district an area of near-universal insecticide-treated mosquito net coverage. Am. J. Tropical Med. Hyg. 84(1), 152-157 (2011).
8. Yeka A, Gasasira A, Mpimbaza A et al. Malaria in Uganda: challenges to control on the long road to elimination: I. Epidemiology and current control efforts. Acta Trop. 121(3), 184-195 (2012).
9. Griffin JT, Hollingsworth TD, Okell LC et al. Reducing Plasmodium falciparum malaria transmission in Africa: a modelbased evaluation of intervention strategies. PLoS Med. 7(8), pii: e1000324 (2010).
10. Tatem AJ, Smith DL, Gething PW, Kabaria CW, Snow RW, Hay SI. Ranking of elimination feasibility between malaria-endemic countries. Lancet 376(9752), 1579-1591 (2010).
11. Ogutu BR, Baiden R, Diallo D, Smith PG, Binka FN. Sustainable development of a GCP-compliant clinical trials platform in Africa: the malaria clinical trials alliance perspective. Malar. J. 9, 103 (2010).
12. Khatib RA, Skarbinski J, Njau JD et al. Routine delivery of artemisinin-based combination treatment at fixed health facilities reduces malaria prevalence in Tanzania: an observational study. Malar. J. 11, 140 (2012).
13. Moonen B, Cohen JM, Snow RW et al. Operational strategies to achieve and maintain malaria elimination. Lancet 376(9752), 1592-1603 (2010).
14. Okell LC, Ghani AC, Lyons E, Drakeley CJ. Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J. Infect. Dis. 200(10), 1509-1517 (2009).
15. Warrell DA, Gilles HM. Essential Malariology. Hodder Arnold, London, UK (2002).
16. Liu Z, Miao J, Cui L. Gametocytogenesis in malaria parasite: commitment, development and regulation. Future Microbiol. 6(11), 1351-1369 (2011).
17. Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin. Microbiol. Rev. 24(2), 377-410 (2011).
18. Ratcliff A, Siswantoro H, Kenangalem E et al. Two fixed-dose artemisinin combinations for drug-resistant falciparum and vivax malaria in Papua, Indonesia: an openlabel randomised comparison. Lancet 369(9563), 757-765 (2007).
19. Paaijmans KP, Read AF, Thomas MB. Understanding the link between malaria risk and climate. Proc. Natl Acad. Sci. USA 106(33), 13844-13849 (2009).
20. Boyd MF. Studies on Plasmodium vivax. 2. The influence of temperature on the duration of the extrinsic incubation period. Am. J. Epidemiol. 16, 851-853 (1932).
21. Filipe JA, Riley EM, Drakeley CJ, Sutherland CJ, Ghani AC. Determination of the processes driving the acquisition of immunity to malaria using a mathematical transmission model. PLoS Comput. Biol. 3(12), e255 (2007).
22. Smith T, Felger I, Tanner M, Beck HP. Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Trans. R. Soc. Trop. Med. Hyg. 93(Suppl. 1), 59-64 (1999).
23. Magesa SM, Mdira KY, Babiker HA et al. Diversity of Plasmodium falciparum clones infecting children living in a holoendemic area in north-eastern Tanzania. Acta Trop. 84(2), 83-92 (2002).
24. Hamad AA, El Hassan IM, El Khalifa AA et al. Chronic Plasmodium falciparum infections in an area of low intensity malaria transmission in the Sudan. Parasitology 120(Pt 5), 447-456 (2000).
25. Michon P, Cole-Tobian JL, Dabod E et al. The risk of malarial infections and disease in Papua New Guinean children. Am. J. Trop. Med. Hyg. 76(6), 997-1008 (2007).
26. Lin E, Kiniboro B, Gray L et al. Differential patterns of infection and disease with P. falciparum and P. vivax in young Papua New Guinean children. PLoS ONE 5(2), e9047 (2010).
27. Smith T, Schellenberg JA, Hayes R. Attributable fraction estimates and case definitions for malaria in endemic areas. Stat. Med. 13(22), 2345-2358 (1994).
28. Lievens M, Aponte JJ, Williamson J et al. Statistical methodology for the evaluation of vaccine efficacy in a Phase III multicentre trial of the RTS, S/AS01 malaria vaccine in African children. Malar. J. 10, 222 (2011).
29. Laishram DD, Sutton PL, Nanda N et al. The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malar. J. 11, 29 (2012).
30. Alves FP, Gil LH, Marrelli MT, Ribolla PE, Camargo EP, Da Silva LH. Asymptomatic carriers of Plasmodium spp. as infection source for malaria vector mosquitoes in the Brazilian Amazon. J. Med. Entomol. 42(5), 777-779 (2005).
31. Ouédraogo AL, Bousema T, de Vlas SJ et al. The plasticity of Plasmodium falciparum gametocytaemia in relation to age in Burkina Faso. Malar. J. 9, 281 (2010).
32. Bousema T, Okell L, Shekalaghe S et al. Revisiting the circulation time of Plasmodium falciparum gametocytes: molecular detection methods to estimate the duration of gametocyte carriage and the effect of gametocytocidal drugs. Malar. J. 9, 136 (2010).
33. Mabunda S, Aponte JJ, Tiago A, Alonso P. A country-wide malaria survey in Mozambique. II. Malaria attributable proportion of fever and establishment of malaria case definition in children across different epidemiological settings. Malar. J. 8, 74 (2009).
34. Gonçalves RM, Scopel KK, Bastos MS, Ferreira MU. Cytokine balance in human malaria: does Plasmodium vivax elicit more inflammatory responses than Plasmodium falciparum? PLoS ONE 7(9), e44394 (2012).
35. Roper C, Elhassan IM, Hviid L et al. Detection of very low level Plasmodium falciparum infections using the nested polymerase chain reaction and a reassessment of the epidemiology of unstable malaria in Sudan. Am. J. Trop. Med. Hyg. 54(4), 325-331 (1996).
36. Snounou G, Pinheiro L, Gonçalves A et al. The importance of sensitive detection of malaria parasites in the human and insect hosts in epidemiological studies, as shown by the analysis of field samples from Guinea Bissau. Trans. R. Soc. Trop. Med. Hyg. 87(6), 649-653 (1993).
37. French N, Nakiyingi J, Lugada E, Watera C, Whitworth JA, Gilks CF. Increasing rates of malarial fever with deteriorating immune status in HIV-1-infected Ugandan adults. AIDS 15(7), 899-906 (2001).
38. Nacher M. Helminth-infected patients with malaria: a low profile transmission hub? Malar. J. 11, 376 (2012).
39. Diallo TO, Remoue F, Gaayeb L et al. Schistosomiasis coinfection in children influences acquired immune response against Plasmodium falciparum malaria antigens. PLoS ONE 5(9), e12764 (2010).
40. Lyke KE, Wang A, Dabo A et al. Antigenspecific B memory cell responses to Plasmodium falciparum malaria antigens and Schistosoma haematobium antigens in co-infected Malian children. PLoS ONE 7(6), e37868 (2012).
41. Courtin D, Djilali-Saïah A, Milet J et al. Schistosoma haematobium infection affects Plasmodium falciparum-specific IgG responses associated with protection against malaria. Parasite Immunol. 33(2), 124-131 (2011).
42. Sangweme DT, Midzi N, Zinyowera-Mutapuri S, Mduluza T, Diener-West M, Kumar N. Impact of schistosome infection on Plasmodium falciparum malariometric indices and immune correlates in school age children in Burma Valley, Zimbabwe. PLoS Negl. Trop. Dis. 4(11), e882 (2010).
43. Wongsrichanalai C, Barcus MJ, Muth S, Sutamihardja A, Wernsdorfer WH. A review of malaria diagnostic tools: microscopy and rapid diagnostic test (RDT). Am. J. Trop. Med. Hyg. 77(Suppl. 6), 119-127 (2007).
44. Hopkins H, Kambale W, Kamya MR, Staedke SG, Dorsey G, Rosenthal PJ. Comparison of HRP2-and pLDH-based rapid diagnostic tests for malaria with longitudinal follow-up in Kampala, Uganda. Am. J. Trop. Med. Hyg. 76(6), 1092-1097 (2007).
45. Moody A. Rapid diagnostic tests for malaria parasites. Clin. Microbiol. Rev. 15(1), 66-78 (2002).
46. Mahajan B, Zheng H, Pham PT et al. Polymerase chain reaction-based tests for pan-species and species-specific detection of human Plasmodium parasites. Transfusion 52(9), 1949-1956 (2012).
47. Stresman G, Kobayashi T, Kamanga A et al. Malaria research challenges in low prevalence settings. Malar. J. 11, 353 (2012).
48. Scuracchio P, Vieira SD, Dourado DA et al. Transfusion-transmitted malaria: case report of asymptomatic donor harboring Plasmodium malariae. Rev. Inst. Med. Trop. São Paulo 53(1), 55-59 (2011).
49. Rojo-Marcos G, Cuadros-Gonzalez J, Gete-Garcia L et al. [Plasmodium ovale infection: description of 16 cases and a review]. Enfermedades Infecciosas Y Microbiologia Clinica 29(3), 204-208 (2011).
50. da Silva-Nunes M, Ferreira MU. Clinical spectrum of uncomplicated malaria in semi-immune Amazonians: beyond the 'symptomatic' vs 'asymptomatic' dichotomy. Memorias Do Instituto Oswaldo Cruz 102(3), 341-347 (2007).
51. Harris I, Sharrock WW, Bain LM et al. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar. J. 9, 254 (2010).
52. Hoyer S, Nguon S, Kim S et al. Focused Screening and Treatment (FSAT): a PCR-based strategy to detect malaria parasite carriers and contain drug resistant P. falciparum, Pailin, Cambodia. PLoS ONE 7(10), e45797 (2012).
53. Alves FP, Durlacher RR, Menezes MJ, Krieger H, Silva LH, Camargo EP. High prevalence of asymptomatic Plasmodium vivax and Plasmodium falciparum infections in native Amazonian populations. Am. J. Trop. Med. Hyg. 66(6), 641-648 (2002).
54. Bereczky S, Montgomery SM, Troye-Blomberg M, Rooth I, Shaw MA, Färnert A. Elevated anti-malarial IgE in asymptomatic individuals is associated with reduced risk for subsequent clinical malaria. Int. J. Parasitol. 34(8), 935-942 (2004).
55. Nsobya SL, Parikh S, Kironde F et al. Molecular evaluation of the natural history of asymptomatic parasitemia in Ugandan children. J. Infect. Dis. 189(12), 2220-2226 (2004).
56. Kun JF, Missinou MA, Lell B et al. New emerging Plasmodium falciparum genotypes in children during the transition phase from asymptomatic parasitemia to malaria. Am. J. Trop. Med. Hyg. 66(6), 653-658 (2002).
57. Rieckmann KH. Asymptomatic malaria. Lancet 1(7637), 82-83 (1970).
58. Felger I, Maire M, Bretscher MT et al. The dynamics of natural Plasmodium falciparum infections. PLoS ONE 7(9), e45542 (2012).
59. McCarra MB, Ayodo G, Sumba PO et al. Antibodies to Plasmodium falciparum erythrocyte-binding antigen-175 are associated with protection from clinical malaria. Pediatr. Infect. Dis. J. 30(12), 1037-1042 (2011).
60. Babiker HA, Abdel-Muhsin AM, Ranford-Cartwright LC, Satti G, Walliker D. Characteristics of Plasmodium falciparum parasites that survive the lengthy dry season in eastern Sudan where malaria transmission is markedly seasonal. Am. J. Trop. Med. Hyg. 59(4), 582-590 (1998).
61. Vinetz JM, Li J, McCutchan TF, Kaslow DC. Plasmodium malariae infection in an asymptomatic 74-year-old Greek woman with splenomegaly. N. Engl. J. Med. 338(6), 367-371 (1998).
62. Bousema JT, Gouagna LC, Meutstege AM et al. Treatment failure of pyrimethamine-sulphadoxine and induction of Plasmodium falciparum gametocytaemia in children in western Kenya. Trop. Med. Int. Health 8(5), 427-430 (2003).
63. Price R, Nosten F, Simpson JA et al. Risk factors for gametocyte carriage in uncomplicated falciparum malaria. Am. J. Trop. Med. Hyg. 60(6), 1019-1023 (1999).
64. von Seidlein L, Drakeley C, Greenwood B, Walraven G, Targett G. Risk factors for gametocyte carriage in Gambian children. Am. J. Trop. Med. Hyg. 65(5), 523-527 (2001).
65. Sowunmi A, Fateye BA, Adedeji AA, Fehintola FA, Happi TC. Risk factors for gametocyte carriage in uncomplicated falciparum malaria in children. Parasitology 129(Pt 3), 255-262 (2004).
66. Lima NF, Bastos MS, Ferreira MU. Plasmodium vivax: reverse transcriptase real-time PCR for gametocyte detection and quantitation in clinical samples. Exp. Parasitol. 132(3), 348-354 (2012).
67. Gouagna LC, Ferguson HM, Okech BA et al. Plasmodium falciparum malaria disease manifestations in humans and transmission to Anopheles gambiae: a field study in western Kenya. Parasitology 128(Pt 3), 235-243 (2004).
68. Bousema T, Dinglasan RR, Morlais I et al. Mosquito feeding assays to determine the infectiousness of naturally infected Plasmodium falciparum gametocyte carriers. PLoS ONE 7(8), e42821 (2012).
69. White NJ. The role of anti-malarial drugs in eliminating malaria. Malar. J. 7(Suppl. 1), S8 (2008).
70. Schneider P, Bousema JT, Gouagna LC et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am. J. Trop. Med. Hyg. 76(3), 470-474 (2007).
71. Lacroix R, Mukabana WR, Gouagna LC, Koella JC. Malaria infection increases attractiveness of humans to mosquitoes. PLoS Biol. 3(9), e298 (2005).
72. Ghani AC, Sutherland CJ, Riley EM et al. Loss of population levels of immunity to malaria as a result of exposure-reducing interventions: consequences for interpretation of disease trends. PLoS ONE 4(2), e4383 (2009).
73. Macauley C. Aggressive active case detection: a malaria control strategy based on the Brazilian model. Soc. Sci. Med. 60(3), 563-573 (2005).
74. Bousema JT, Gouagna LC, Drakeley CJ et al. Plasmodium falciparum gametocyte carriage in asymptomatic children in western Kenya. Malar. J. 3, 18 (2004).
75. Manjurano A, Okell L, Lukindo T et al. Association of sub-microscopic malaria parasite carriage with transmission intensity in north-eastern Tanzania. Malar. J. 10, 370 (2011).
76. Gosling RD, Okell L, Mosha J, Chandramohan D. The role of antimalarial treatment in the elimination of malaria. Clin. Microbiol. Infect. 17(11), 1617-1623 (2011).
77. Kern SE, Tiono AB, Makanga M et al. Community screening and treatment of asymptomatic carriers of Plasmodium falciparum with artemether-lumefantrine to reduce malaria disease burden: a modelling and simulation analysis. Malar. J. 10, 210 (2011).
78. Okell LC, Griffin JT, Kleinschmidt I et al. The potential contribution of mass treatment to the control of Plasmodium falciparum malaria. PLoS ONE 6(5), e20179 (2011).
79. Snowden F. The Conquest of Malaria: Italy, 1900-1962. Yale University Press, CT, USA (2006).
80. von Seidlein L, Greenwood BM. Mass administrations of antimalarial drugs. Trends Parasitol. 19(10), 452-460 (2003).
81. Kaneko A, Taleo G, Kalkoa M, Yamar S, Kobayakawa T, Björkman A. Malaria eradication on islands. Lancet 356(9241), 1560-1564 (2000).
82. Garfield RM, Vermund SH. Changes in malaria incidence after mass drug administration in Nicaragua. Lancet 2(8348), 500-503 (1983).
83. von Seidlein L, Walraven G, Milligan PJ et al. The effect of mass administration of sulfadoxine-pyrimethamine combined with artesunate on malaria incidence: a double-blind, community-randomized, placebo-controlled trial in The Gambia. Trans. R. Soc. Trop. Med. Hyg. 97(2), 217-225 (2003).
84. Shekalaghe SA, Drakeley C, van den Bosch S et al. A cluster-randomized trial of mass drug administration with a gametocytocidal drug combination to interrupt malaria transmission in a low endemic area in Tanzania. Malar. J. 10, 247 (2011).
85. Song J, Socheat D, Tan B et al. Rapid and effective malaria control in Cambodia through mass administration of artemisinin-piperaquine. Malar. J. 9, 57 (2010).
86. Yekutiel P. Problems of epidemiology in malaria eradication. Bull. World Health Organ. 22, 669-683 (1960).
87. Bruce-Chwatt LJ. Malaria research and eradication in the USSR. A review of Soviet achievements in the field of malariology. Bull. World Health Organ. 21, 737-772 (1959).
88. Nájera JA, González-Silva M, Alonso PL. Some lessons for the future from the Global Malaria Eradication Programme ( 1955-1969). PLoS Med. 8(1), e1000412 (2011).
89. Kidson C, Indaratna K. Ecology, economics and political will: the vicissitudes of malaria strategies in Asia. Parassitologia 40(1-2), 39-46 (1998).
90. Molteni F, Anderegg C, Ali A et al. Is active malaria case detection in the community able to inhibit low-level focal malaria transmission in Zanzibar? Presented at: American Society of Tropical Medicine and Hygiene 60th Annual Meeting. PA, USA, 4-8 December 2011 (Abstract 676).
91. Stresman GH, Kamanga A, Moono P et al. A method of active case detection to target reservoirs of asymptomatic malaria and gametocyte carriers in a rural area in Southern Province, Zambia. Malar. J. 9, 265 (2010).
92. Abdel-Latif MS, Dietz K, Issifou S, Kremsner PG, Klinkert MQ. Antibodies to Plasmodium falciparum rifin proteins are associated with rapid parasite clearance and asymptomatic infections. Infect. Immun. 71(11), 6229-6233 (2003).
93. Rottmann M, Lavstsen T, Mugasa JP et al. Differential expression of var gene groups is associated with morbidity caused by Plasmodium falciparum infection in Tanzanian children. Infect. Immun. 74(7), 3904-3911 (2006).
94. Alves FP, Durlacher RR, Menezes MJ, Krieger H, Silva LH, Camargo EP. High prevalence of asymptomatic Plasmodium vivax and Plasmodium falciparum infections in native Amazonian populations. Am. J. Trop. Med. Hyg. 66(6), 641-648 (2002).
95. Cucunubá ZM, Guerra AP, Rahirant SJ, Rivera JA, Cortés LJ, Nicholls RS. Asymptomatic Plasmodium spp. infection in Tierralta, Colombia. Mem. Inst. Oswaldo Cruz 103(7), 668-673 (2008).
96. Boutlis CS, Tjitra E, Maniboey H et al. Nitric oxide production and mononuclear cell nitric oxide synthase activity in malaria-tolerant Papuan adults. Infect. Immun. 71(7), 3682-3689 (2003).
97. de Mast Q, Syafruddin D, Keijmel S et al. Increased serum hepcidin and alterations in blood iron parameters associated with asymptomatic P. falciparum and P. vivax malaria. Haematologica 95(7), 1068-1074 (2010).
98. Fernando SD, Abeyasinghe RR, Galappaththy GN, Rajapaksa LC. Absence of asymptomatic malaria infections in previously high endemic areas of Sri Lanka. Am. J. Trop. Med. Hyg. 81(5), 763-767 (2009).
99. Turki H, Zoghi S, Mehrizi AA et al. Absence of asymptomatic malaria infection in endemic area of Bashagard district, Hormozgan province, Iran. Iran. J. Parasitol. 7(1), 36-44 (2012).
100. Zoghi S, Mehrizi AA, Raeisi A et al. Survey for asymptomatic malaria cases in low transmission settings of Iran under elimination programme. Malar. J. 11, 126 (2012).
101. Atkinson JA, Johnson ML, Wijesinghe R et al. Operational research to inform a sub-national surveillance intervention for malaria elimination in Solomon Islands. Malar. J. 11, 101 (2012).
102. Kumudunayana WM, Gunasekera TDW, Abeyasinghe RR, Premawansa S, Fernando SD. Usefulness of polymerase chain reaction to supplement field microscopy in a pre-selected population with a high probability of malaria infections. Am. J. Trop. Med. Hyg. 85(1), 6-11 (2011).
103. Congpuong K, Saejeng A, Sug-Aram R et al. Mass blood survey for malaria: pooling and real-time PCR combined with expert microscopy in north-west Thailand. Malar. J. 11, 288 (2012).
104. Diallo A, Ndam NT, Moussiliou A et al. Asymptomatic carriage of Plasmodium in urban Dakar: the risk of malaria should not be underestimated. PLoS ONE 7(2), e31100 (2012).
105. Eisele TP, Miller JM, Moonga HB, Hamainza B, Hutchinson P, Keating J. Malaria infection and anemia prevalence in Zambia's Luangwa District: an area of near-universal insecticide-treated mosquito net coverage. Am. J. Trop. Med. Hyg. 84(1), 152-157 (2011).
106. Barracks G, Atkins C, Auliff A et al. Malaria on isolated Melanesian islands prior to the initiation of malaria elimination activities. Malaria Journal. 9, (2010).
107. Hsiang MS, Lin M, Dokomajilar C et al. PCR-based pooling of dried blood spots for detection of malaria parasites: optimization and application to a cohort of Ugandan children. J. Clin. Microbiol. 48(10), 3539-3543 (2010).
108. da Silva NS, da Silva-Nunes M, Malafronte RS et al. Epidemiology and control of frontier malaria in Brazil: lessons from community-based studies in rural Amazonia. Trans. R. Soc. Trop. Med. Hyg. 104(5), 343-350 (2010).
109. Kritsiriwuthinan K, Ngrenngarmlert W. Molecular screening of Plasmodium infections among migrant workers in Thailand. J. Vector Borne Dis. 48(4), 214-218 (2011).
110. Roper C, Richardson W, Elhassan IM et al. Seasonal changes in the Plasmodium falciparum population in individuals and their relationship to clinical malaria: a longitudinal study in a Sudanese village. Parasitology 116 (Pt 6), 501-510 (1998).
111. Rodulfo H, de Donato M, Quijada I, Peña A. High prevalence of malaria infection in Amazonas State, Venezuela. Rev. Inst. Med. Trop. São Paulo 49(2), 79-85 (2007).
112. Gahutu JB, Steininger C, Shyirambere C et al. Prevalence and risk factors of malaria among children in southern highland Rwanda. Malar. J. 10, 134 (2011).
113. Katsuragawa TH, Gil LH, Tada MS et al. The dynamics of transmission and spatial distribution of malaria in riverside areas of Porto Velho, Rondônia, in the Amazon region of Brazil. PLoS ONE 5(2), e9245 (2010).
114. Camargo EP, Alves F, Pereira da Silva LH. Symptomless Plasmodium vivax infections in native Amazonians. Lancet 353(9162), 1415-1416 (1999).
115. Färnert A, Williams TN, Mwangi TW et al. Transmission-dependent tolerance to multiclonal Plasmodium falciparum infection. J. Infect. Dis. 200(7), 1166-1175 (2009).
116. Ladeia-Andrade S, Ferreira MU, de Carvalho ME, Curado I, Coura JR. Age-dependent acquisition of protective immunity to malaria in riverine populations of the Amazon Basin of Brazil. Am. J. Trop. Med. Hyg. 80(3), 452-459 (2009).
117. Vafa M, Troye-Blomberg M, Anchang J, Garcia A, Migot-Nabias F. Multiplicity of Plasmodium falciparum infection in asymptomatic children in Senegal: relation to transmission, age and erythrocyte variants. Malar. J. 7, 17 (2008).
118. Suarez-Mutis MC, Coura JR. Changes in the epidemiological pattern of malaria in a rural area of the middle Rio Negro, Brazilian Amazon: a retrospective analysis. Cad. Saude Publica 23(4), 795-804 (2007).
119. Baliraine FN, Afrane YA, Amenya DA et al. High prevalence of asymptomatic Plasmodium falciparum infections in a highland area of western Kenya: a cohort study. J. Infect. Dis. 200(1), 66-74 (2009).
120. Pinto J, Sousa CA, Gil V et al. Malaria in São Tomé and Príncipe: parasite prevalences and vector densities. Acta Trop. 76(2), 185-193 (2000).
121. Crookston BT, Alder SC, Boakye I et al. Exploring the relationship between chronic undernutrition and asymptomatic malaria in Ghanaian children. Malar. J. 9, 39 (2010).
122. Liljander A, Bejon P, Mwacharo J et al. Clearance of asymptomatic P. falciparum infections interacts with the number of clones to predict the risk of subsequent malaria in Kenyan children. PLoS ONE 6(2), e16940 (2011).
123. Koukouikila-Koussounda F, Malonga V, Mayengue PI, Ndounga M, Vouvoungui CJ, Ntoumi F. Genetic polymorphism of merozoite surface protein 2 and prevalence of K76T Pfcrt mutation in Plasmodium falciparum field isolates from Congolese children with asymptomatic infections. Malar. J. 11, 105 (2012).
124. Bereczky S, Liljander A, Rooth I et al. Multiclonal asymptomatic Plasmodium falciparum infections predict a reduced risk of malaria disease in a Tanzanian population. Microbes Infect. 9(1), 103-110 (2007).
125. Dal-Bianco MP, Köster KB, Kombila UD et al. High prevalence of asymptomatic Plasmodium falciparum infection in Gabonese adults. Am. J. Trop. Med. Hyg. 77(5), 939-942 (2007).
126. Owusu-Agyei S, Smith T, Beck HP, Amenga-Etego L, Felger I. Molecular epidemiology of Plasmodium falciparum infections among asymptomatic inhabitants of a holoendemic malarious area in northern Ghana. Trop. Med. Int. Health 7(5), 421-428 (2002).
127. Rajagopalan PK, Das PK, Pani SP et al. Parasitological aspects of malaria persistence in Koraput district Orissa, India. Indian J. Med. Res. 91, 44-51 (1990).
128. González JM, Olano V, Vergara J et al. Unstable, low-level transmission of malaria on the Colombian Pacific Coast. Ann. Trop. Med. Parasitol. 91(4), 349-358 (1997).
129. Mato SP. Anemia and malaria in a Yanomami Amerindian population from the southern Venezuelan Amazon. Am. J. Trop. Med. Hyg. 59(6), 998-1001 (1998).
130. Anothay O, Pongvongsa T. Childhood malaria in the Lao People's Democratic Republic. Bull. World Health Organ. 76(Suppl. 1), 29-34 (1998).
131. Geiger C, Agustar HK, Compaoré G et al. Declining malaria parasite prevalence and trends of asymptomatic parasitaemia in a seasonal transmission setting in northwestern Burkina Faso between 2000 and 2009-2012. Malar. J. 12(1), 27 (2013).
132. Eisele TP, Keating J, Bennett A et al. Prevalence of Plasmodium falciparum infection in rainy season, Artibonite Valley, Haiti, 2006. Emerging Infect. Dis. 13(10), 1494-1496 (2007).