Skip to main content
Top
Published in: Malaria Journal 1/2013

Open Access 01-12-2013 | Research

Assessing malaria transmission in a low endemicity area of north-western Peru

Authors: Angel Rosas-Aguirre, Alejandro Llanos-Cuentas, Niko Speybroeck, Jackie Cook, Juan Contreras-Mancilla, Veronica Soto, Dionicia Gamboa, Edwar Pozo, Oscar J Ponce, Mayne O Pereira, Irene S Soares, Michael Theisen, Umberto D’Alessandro, Annette Erhart

Published in: Malaria Journal | Issue 1/2013

Login to get access

Abstract

Background

Where malaria endemicity is low, control programmes need increasingly sensitive tools for monitoring malaria transmission intensity (MTI) and to better define health priorities. A cross-sectional survey was conducted in a low endemicity area of the Peruvian north-western coast to assess the MTI using both molecular and serological tools.

Methods

Epidemiological, parasitological and serological data were collected from 2,667 individuals in three settlements of Bellavista district, in May 2010. Parasite infection was detected using microscopy and polymerase chain reaction (PCR). Antibodies to Plasmodium vivax merozoite surface protein-119 (PvMSP119) and to Plasmodium falciparum glutamate-rich protein (PfGLURP) were detected by ELISA. Risk factors for exposure to malaria (seropositivity) were assessed by multivariate survey logistic regression models. Age-specific antibody prevalence of both P. falciparum and P. vivax were analysed using a previously published catalytic conversion model based on maximum likelihood for generating seroconversion rates (SCR).

Results

The overall parasite prevalence by microscopy and PCR were extremely low: 0.3 and 0.9%, respectively for P. vivax, and 0 and 0.04%, respectively for P. falciparum, while seroprevalence was much higher, 13.6% for P. vivax and 9.8% for P. falciparum. Settlement, age and occupation as moto-taxi driver during previous year were significantly associated with P. falciparum exposure, while age and distance to the water drain were associated with P. vivax exposure. Likelihood ratio tests supported age seroprevalence curves with two SCR for both P. vivax and P. falciparum indicating significant changes in the MTI over time. The SCR for PfGLURP was 19-fold lower after 2002 as compared to before (λ1 = 0.022 versus λ2 = 0.431), and the SCR for PvMSP119 was four-fold higher after 2006 as compared to before (λ1 = 0.024 versus λ2 = 0.006).

Conclusion

Combining molecular and serological tools considerably enhanced the capacity of detecting current and past exposure to malaria infections and related risks factors in this very low endemicity area. This allowed for an improved characterization of the current human reservoir of infections, largely hidden and heterogeneous, as well as providing insights into recent changes in species specific MTIs. This approach will be of key importance for evaluating and monitoring future malaria elimination strategies.
Appendix
Available only for authorised users
Literature
1.
go back to reference WHO Global Malaria Programme: World malaria report 2011. 2011, Geneva: WHO WHO Global Malaria Programme: World malaria report 2011. 2011, Geneva: WHO
2.
go back to reference Roberts DR, Laughlin LL, Hsheih P, Legters LJ: DDT, global strategies, and a malaria control crisis in South America. Emerg Infect Dis. 1997, 3: 295-302. 10.3201/eid0303.970305.PubMedCentralCrossRefPubMed Roberts DR, Laughlin LL, Hsheih P, Legters LJ: DDT, global strategies, and a malaria control crisis in South America. Emerg Infect Dis. 1997, 3: 295-302. 10.3201/eid0303.970305.PubMedCentralCrossRefPubMed
3.
go back to reference Marquiño W, MacArthur JR, Barat LM, Oblitas FE, Arrunátegui M, Garavito G, Chafloque ML, Pardavé B, Gutierrez S, Arróspide N, Carrillo C, Cabezas C, Ruebush TK: Efficacy of chloroquine, sulfadoxine-pyrimethamine, and mefloquine for the treatment of uncomplicated Plasmodium falciparum malaria on the north coast of Peru. Am J Trop Med Hyg. 2003, 68: 120-123.PubMed Marquiño W, MacArthur JR, Barat LM, Oblitas FE, Arrunátegui M, Garavito G, Chafloque ML, Pardavé B, Gutierrez S, Arróspide N, Carrillo C, Cabezas C, Ruebush TK: Efficacy of chloroquine, sulfadoxine-pyrimethamine, and mefloquine for the treatment of uncomplicated Plasmodium falciparum malaria on the north coast of Peru. Am J Trop Med Hyg. 2003, 68: 120-123.PubMed
4.
go back to reference Marquiño W, Huilca M, Calampa C, Falconí E, Cabezas C, Naupay R, Ruebush TK: Efficacy of mefloquine and a mefloquine-artesunate combination therapy for the treatment of uncomplicated Plasmodium falciparum malaria in the Amazon Basin of Peru. Am J Trop Med Hyg. 2003, 68: 608-612.PubMed Marquiño W, Huilca M, Calampa C, Falconí E, Cabezas C, Naupay R, Ruebush TK: Efficacy of mefloquine and a mefloquine-artesunate combination therapy for the treatment of uncomplicated Plasmodium falciparum malaria in the Amazon Basin of Peru. Am J Trop Med Hyg. 2003, 68: 608-612.PubMed
5.
go back to reference Aramburu J, Ramal C, Witzig R: Malaria reemergence in the Peruvian Amazon region. Emerg Infect Dis. 2009, 5: 209-215. Aramburu J, Ramal C, Witzig R: Malaria reemergence in the Peruvian Amazon region. Emerg Infect Dis. 2009, 5: 209-215.
6.
go back to reference Gagnon AS, Smoyer-Tomic KE, Bush ABG: The El Niño southern oscillation and malaria epidemics in South America. Int J Biometeorol. 2002, 46: 81-89. 10.1007/s00484-001-0119-6.CrossRefPubMed Gagnon AS, Smoyer-Tomic KE, Bush ABG: The El Niño southern oscillation and malaria epidemics in South America. Int J Biometeorol. 2002, 46: 81-89. 10.1007/s00484-001-0119-6.CrossRefPubMed
8.
go back to reference Williams HA, Vincent-Mark A, Herrera Y, Chang OJ: A retrospective analysis of the change in anti-malarial treatment policy: Peru. Malar J. 2009, 8: 85-10.1186/1475-2875-8-85.PubMedCentralCrossRefPubMed Williams HA, Vincent-Mark A, Herrera Y, Chang OJ: A retrospective analysis of the change in anti-malarial treatment policy: Peru. Malar J. 2009, 8: 85-10.1186/1475-2875-8-85.PubMedCentralCrossRefPubMed
9.
go back to reference Flores W, Chang J, Barillas E: Rapid assessment of the performance of malaria control strategies implemented by countries in the Amazon subregion using adequacy criteria: case study. Malar J. 2011, 10: 379-10.1186/1475-2875-10-379.PubMedCentralCrossRefPubMed Flores W, Chang J, Barillas E: Rapid assessment of the performance of malaria control strategies implemented by countries in the Amazon subregion using adequacy criteria: case study. Malar J. 2011, 10: 379-10.1186/1475-2875-10-379.PubMedCentralCrossRefPubMed
10.
go back to reference Rosas-Aguirre A, Guzmán-Guzmán M, Moreno-Gutierrez D, Rodriguez-Ferrucci H, Vargas-Pacherrez D, Acuña-González Y: Long-lasting insecticide - treated bednet ownership, retention and usage one year after their distribution in Loreto, Peru. Rev Peru Med Exp Salud Publica. 2011, 28: 228-236. 10.1590/S1726-46342011000200009.CrossRefPubMed Rosas-Aguirre A, Guzmán-Guzmán M, Moreno-Gutierrez D, Rodriguez-Ferrucci H, Vargas-Pacherrez D, Acuña-González Y: Long-lasting insecticide - treated bednet ownership, retention and usage one year after their distribution in Loreto, Peru. Rev Peru Med Exp Salud Publica. 2011, 28: 228-236. 10.1590/S1726-46342011000200009.CrossRefPubMed
11.
go back to reference Hay SI, Smith DL, Snow RW: Measuring malaria endemicity from intense to interrupted transmission. Lancet Infect Dis. 2008, 8: 369-378. 10.1016/S1473-3099(08)70069-0.PubMedCentralCrossRefPubMed Hay SI, Smith DL, Snow RW: Measuring malaria endemicity from intense to interrupted transmission. Lancet Infect Dis. 2008, 8: 369-378. 10.1016/S1473-3099(08)70069-0.PubMedCentralCrossRefPubMed
12.
go back to reference Greenwood BM: Control to elimination: implications for malaria research. Trends Parasitol. 2008, 24: 449-454. 10.1016/j.pt.2008.07.002.CrossRefPubMed Greenwood BM: Control to elimination: implications for malaria research. Trends Parasitol. 2008, 24: 449-454. 10.1016/j.pt.2008.07.002.CrossRefPubMed
13.
go back to reference Byass P: Making sense of long-term changes in malaria. Lancet. 2008, 372: 1523-1525. 10.1016/S0140-6736(08)61631-1.CrossRefPubMed Byass P: Making sense of long-term changes in malaria. Lancet. 2008, 372: 1523-1525. 10.1016/S0140-6736(08)61631-1.CrossRefPubMed
14.
go back to reference Elissa N, Migot-Nabias F, Luty A, Renaut A, Touré F, Vaillant M, Lawoko M, Yangari P, Mayombo J, Lekoulou F, Tshipamba P, Moukagni R, Millet P, Deloron P: Relationship between entomological inoculation rate, Plasmodium falciparum prevalence rate, and incidence of malaria attack in rural Gabon. Acta Trop. 2003, 85: 355-361. 10.1016/S0001-706X(02)00266-8.CrossRefPubMed Elissa N, Migot-Nabias F, Luty A, Renaut A, Touré F, Vaillant M, Lawoko M, Yangari P, Mayombo J, Lekoulou F, Tshipamba P, Moukagni R, Millet P, Deloron P: Relationship between entomological inoculation rate, Plasmodium falciparum prevalence rate, and incidence of malaria attack in rural Gabon. Acta Trop. 2003, 85: 355-361. 10.1016/S0001-706X(02)00266-8.CrossRefPubMed
15.
go back to reference 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: 19-10.1186/1475-2875-8-19.PubMedCentralCrossRefPubMed 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: 19-10.1186/1475-2875-8-19.PubMedCentralCrossRefPubMed
16.
go back to reference Steenkeste N, Rogers WO, Okell L, Jeanne I, Incardona S, Duval L, Chy S, Hewitt S, Chou M, Socheat D, Babin FX, Ariey F, Rogier C: Sub-microscopic malaria cases and mixed malaria infection in a remote area of high malaria endemicity in Rattanakiri province, Cambodia: implication for malaria elimination. Malar J. 2010, 9: 108-10.1186/1475-2875-9-108.PubMedCentralCrossRefPubMed Steenkeste N, Rogers WO, Okell L, Jeanne I, Incardona S, Duval L, Chy S, Hewitt S, Chou M, Socheat D, Babin FX, Ariey F, Rogier C: Sub-microscopic malaria cases and mixed malaria infection in a remote area of high malaria endemicity in Rattanakiri province, Cambodia: implication for malaria elimination. Malar J. 2010, 9: 108-10.1186/1475-2875-9-108.PubMedCentralCrossRefPubMed
17.
go back to reference Coura JR, Suárez-Mutis M, Ladeia-Andrade S: A new challenge for malaria control in Brazil: asymptomatic Plasmodium infection–a review. Mem Inst Oswaldo Cruz. 2006, 101: 229-237.PubMed Coura JR, Suárez-Mutis M, Ladeia-Andrade S: A new challenge for malaria control in Brazil: asymptomatic Plasmodium infection–a review. Mem Inst Oswaldo Cruz. 2006, 101: 229-237.PubMed
18.
go back to reference Johnston SP, Pieniazek NJ, Xayavong MV, Slemenda SB, Wilkins PP, Da Silva AJ: PCR as a confirmatory technique for laboratory diagnosis of malaria. J Clin Microbiol. 2006, 44: 1087-1089. 10.1128/JCM.44.3.1087-1089.2006.PubMedCentralCrossRefPubMed Johnston SP, Pieniazek NJ, Xayavong MV, Slemenda SB, Wilkins PP, Da Silva AJ: PCR as a confirmatory technique for laboratory diagnosis of malaria. J Clin Microbiol. 2006, 44: 1087-1089. 10.1128/JCM.44.3.1087-1089.2006.PubMedCentralCrossRefPubMed
19.
go back to reference Taylor SM, Juliano JJ, Trottman PA, Griffin JB, Landis SH, Kitsa P, Tshefu AK, Meshnick SR: High-throughput pooling and real-time PCR-based strategy for malaria detection. J Clin Microbiol. 2010, 48: 512-519. 10.1128/JCM.01800-09.PubMedCentralCrossRefPubMed Taylor SM, Juliano JJ, Trottman PA, Griffin JB, Landis SH, Kitsa P, Tshefu AK, Meshnick SR: High-throughput pooling and real-time PCR-based strategy for malaria detection. J Clin Microbiol. 2010, 48: 512-519. 10.1128/JCM.01800-09.PubMedCentralCrossRefPubMed
20.
go back to reference Corran P, Coleman P, Riley E, Drakeley C: Serology: a robust indicator of malaria transmission intensity?. Trends Parasitol. 2007, 23: 575-582. 10.1016/j.pt.2007.08.023.CrossRefPubMed Corran P, Coleman P, Riley E, Drakeley C: Serology: a robust indicator of malaria transmission intensity?. Trends Parasitol. 2007, 23: 575-582. 10.1016/j.pt.2007.08.023.CrossRefPubMed
21.
go back to reference Williams GS, Mweya C, Stewart L, Mtove G, Reyburn H, Cook J, Corran PH, Riley EM, Drakeley CJ: Immunophoretic rapid diagnostic tests as a source of immunoglobulins for estimating malaria sero-prevalence and transmission intensity. Malar J. 2009, 8: 168-10.1186/1475-2875-8-168.PubMedCentralCrossRefPubMed Williams GS, Mweya C, Stewart L, Mtove G, Reyburn H, Cook J, Corran PH, Riley EM, Drakeley CJ: Immunophoretic rapid diagnostic tests as a source of immunoglobulins for estimating malaria sero-prevalence and transmission intensity. Malar J. 2009, 8: 168-10.1186/1475-2875-8-168.PubMedCentralCrossRefPubMed
22.
go back to reference 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: Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci USA. 2005, 102: 5108-5113. 10.1073/pnas.0408725102.PubMedCentralCrossRefPubMed 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: Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci USA. 2005, 102: 5108-5113. 10.1073/pnas.0408725102.PubMedCentralCrossRefPubMed
23.
go back to reference 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. 10.3201/eid1603.090732.PubMedCentralCrossRefPubMed 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. 10.3201/eid1603.090732.PubMedCentralCrossRefPubMed
24.
go back to reference 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: e6083-10.1371/journal.pone.0006083.PubMedCentralCrossRefPubMed 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: e6083-10.1371/journal.pone.0006083.PubMedCentralCrossRefPubMed
25.
go back to reference 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: e25137-10.1371/journal.pone.0025137.PubMedCentralCrossRefPubMed 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: e25137-10.1371/journal.pone.0025137.PubMedCentralCrossRefPubMed
29.
go back to reference Guthmann JP, Hall AJ, Jaffar S, Palacios A, Lines J, Llanos-Cuentas A: Environmental risk factors for clinical malaria: a case–control study in the Grau region of Peru. Trans R Soc Trop Med Hyg. 2001, 95: 577-583. 10.1016/S0035-9203(01)90084-7.CrossRefPubMed Guthmann JP, Hall AJ, Jaffar S, Palacios A, Lines J, Llanos-Cuentas A: Environmental risk factors for clinical malaria: a case–control study in the Grau region of Peru. Trans R Soc Trop Med Hyg. 2001, 95: 577-583. 10.1016/S0035-9203(01)90084-7.CrossRefPubMed
31.
go back to reference Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE: Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995, 52: 565-568.PubMed Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE: Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995, 52: 565-568.PubMed
32.
go back to reference Rubio JM, Post RJ, Van Leeuwen WMD, Henry MC, Lindergard G, Hommel M: Alternative polymerase chain reaction method to identify Plasmodium species in human blood samples: the semi-nested multiplex malaria PCR (SnM-PCR). Trans R Soc Trop Med Hyg. 2002, 96 (Suppl 1): S199-S204.CrossRefPubMed Rubio JM, Post RJ, Van Leeuwen WMD, Henry MC, Lindergard G, Hommel M: Alternative polymerase chain reaction method to identify Plasmodium species in human blood samples: the semi-nested multiplex malaria PCR (SnM-PCR). Trans R Soc Trop Med Hyg. 2002, 96 (Suppl 1): S199-S204.CrossRefPubMed
33.
go back to reference Cook J, Speybroeck N, Sochanta T, Somony H, Sokny M, Claes F, Lemmens K, Theisen M, Soares IS, D’Alessandro U, Coosemans M, Erhart A: Sero-epidemiological evaluation of changes in Plasmodium falciparum and Plasmodium vivax transmission patterns over the rainy season in Cambodia. Malar J. 2012, 11: 86-10.1186/1475-2875-11-86.PubMedCentralCrossRefPubMed Cook J, Speybroeck N, Sochanta T, Somony H, Sokny M, Claes F, Lemmens K, Theisen M, Soares IS, D’Alessandro U, Coosemans M, Erhart A: Sero-epidemiological evaluation of changes in Plasmodium falciparum and Plasmodium vivax transmission patterns over the rainy season in Cambodia. Malar J. 2012, 11: 86-10.1186/1475-2875-11-86.PubMedCentralCrossRefPubMed
34.
go back to reference Theisen M, Vuust J, Gottschau A, Jepsen S, Høgh B: Antigenicity and immunogenicity of recombinant glutamate-rich protein of Plasmodium falciparum expressed in Escherichia coli. Clin Diagn Lab Immunol. 1995, 2: 30-34.PubMedCentralPubMed Theisen M, Vuust J, Gottschau A, Jepsen S, Høgh B: Antigenicity and immunogenicity of recombinant glutamate-rich protein of Plasmodium falciparum expressed in Escherichia coli. Clin Diagn Lab Immunol. 1995, 2: 30-34.PubMedCentralPubMed
35.
go back to reference Rodrigues MH, Cunha MG, Machado RL, Ferreira OC, Rodrigues MM, Soares IS: Serological detection of Plasmodium vivax malaria using recombinant proteins corresponding to the 19-kDa C-terminal region of the merozoite surface protein-1. Malar J. 2003, 2: 39-10.1186/1475-2875-2-39.PubMedCentralCrossRefPubMed Rodrigues MH, Cunha MG, Machado RL, Ferreira OC, Rodrigues MM, Soares IS: Serological detection of Plasmodium vivax malaria using recombinant proteins corresponding to the 19-kDa C-terminal region of the merozoite surface protein-1. Malar J. 2003, 2: 39-10.1186/1475-2875-2-39.PubMedCentralCrossRefPubMed
36.
go back to reference Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, Griffin J, Cox J, Abeku T, Bousema T, Ghani AC, Drakeley C, Riley E: Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malar J. 2008, 7: 195-10.1186/1475-2875-7-195.PubMedCentralCrossRefPubMed Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, Griffin J, Cox J, Abeku T, Bousema T, Ghani AC, Drakeley C, Riley E: Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malar J. 2008, 7: 195-10.1186/1475-2875-7-195.PubMedCentralCrossRefPubMed
37.
go back to reference 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.PubMed 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.PubMed
38.
go back to reference 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: 169-10.1186/1475-2875-9-169.PubMedCentralCrossRefPubMed 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: 169-10.1186/1475-2875-9-169.PubMedCentralCrossRefPubMed
39.
go back to reference Guthmann JP, Llanos-Cuentas A, Palacios A, Hall AJ: Environmental factors as determinants of malaria risk. A descriptive study on the northern coast of Peru. Trop Med Int Health. 2002, 7: 518-525. 10.1046/j.1365-3156.2002.00883.x.CrossRefPubMed Guthmann JP, Llanos-Cuentas A, Palacios A, Hall AJ: Environmental factors as determinants of malaria risk. A descriptive study on the northern coast of Peru. Trop Med Int Health. 2002, 7: 518-525. 10.1046/j.1365-3156.2002.00883.x.CrossRefPubMed
40.
go back to reference Vinetz JM, Gilman RH: Asymptomatic Plasmodium parasitemia and the ecology of malaria transmission. Am J Trop Med Hyg. 2002, 66: 639-640.PubMed Vinetz JM, Gilman RH: Asymptomatic Plasmodium parasitemia and the ecology of malaria transmission. Am J Trop Med Hyg. 2002, 66: 639-640.PubMed
41.
go back to reference Branch O, Casapia WM, Gamboa DV, Hernandez JN, Alava FF, Roncal N, Alvarez E, Perez EJ, Gotuzzo E: Clustered local transmission and asymptomatic Plasmodium falciparum and Plasmodium vivax malaria infections in a recently emerged, hypoendemic Peruvian Amazon community. Malar J. 2005, 4: 27-10.1186/1475-2875-4-27.PubMedCentralCrossRefPubMed Branch O, Casapia WM, Gamboa DV, Hernandez JN, Alava FF, Roncal N, Alvarez E, Perez EJ, Gotuzzo E: Clustered local transmission and asymptomatic Plasmodium falciparum and Plasmodium vivax malaria infections in a recently emerged, hypoendemic Peruvian Amazon community. Malar J. 2005, 4: 27-10.1186/1475-2875-4-27.PubMedCentralCrossRefPubMed
42.
go back to reference Da Silva-Nunes M, Moreno M, Conn JE, Gamboa D, Abeles S, Vinetz JM, Ferreira MU: Amazonian malaria: asymptomatic human reservoirs, diagnostic challenges, environmentally driven changes in mosquito vector populations, and the mandate for sustainable control strategies. Acta Trop. 2012, 121: 281-291. 10.1016/j.actatropica.2011.10.001.PubMedCentralCrossRefPubMed Da Silva-Nunes M, Moreno M, Conn JE, Gamboa D, Abeles S, Vinetz JM, Ferreira MU: Amazonian malaria: asymptomatic human reservoirs, diagnostic challenges, environmentally driven changes in mosquito vector populations, and the mandate for sustainable control strategies. Acta Trop. 2012, 121: 281-291. 10.1016/j.actatropica.2011.10.001.PubMedCentralCrossRefPubMed
43.
go back to reference 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: Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis. 2010, 201: 1764-1774. 10.1086/652456.CrossRefPubMed 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: Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis. 2010, 201: 1764-1774. 10.1086/652456.CrossRefPubMed
44.
45.
go back to reference Culleton R, Ndounga M, Zeyrek FY, Coban C, Casimiro PN, Takeo S, Tsuboi T, Yadava A, Carter R, Tanabe K: Evidence for the transmission of Plasmodium vivax in the Republic of the Congo, West Central Africa. J Infect Dis. 2009, 200: 1465-1469. 10.1086/644510.CrossRefPubMed Culleton R, Ndounga M, Zeyrek FY, Coban C, Casimiro PN, Takeo S, Tsuboi T, Yadava A, Carter R, Tanabe K: Evidence for the transmission of Plasmodium vivax in the Republic of the Congo, West Central Africa. J Infect Dis. 2009, 200: 1465-1469. 10.1086/644510.CrossRefPubMed
46.
go back to reference Mutapi F, Roussilhon C, Mduluza T, Druilhe P: Anti-malaria humoral responses in children exposed to Plasmodium falciparum and Schistosoma haematobium. Mem Inst Oswaldo Cruz. 2007, 102: 405-409. 10.1590/S0074-02762007005000046.CrossRefPubMed Mutapi F, Roussilhon C, Mduluza T, Druilhe P: Anti-malaria humoral responses in children exposed to Plasmodium falciparum and Schistosoma haematobium. Mem Inst Oswaldo Cruz. 2007, 102: 405-409. 10.1590/S0074-02762007005000046.CrossRefPubMed
47.
go back to reference Bellina C, Castillo C, Puel L, Seminario A, Yerén C: Malaria por Plasmodium falciparum en Sullana. Bol Soc Peru Med Interna. 1999, 12: 163-165. Bellina C, Castillo C, Puel L, Seminario A, Yerén C: Malaria por Plasmodium falciparum en Sullana. Bol Soc Peru Med Interna. 1999, 12: 163-165.
49.
go back to reference Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Lozano WS, Pinedo-Cancino V, Patz JA: The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of Falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg. 2006, 74: 3-11.PubMed Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Lozano WS, Pinedo-Cancino V, Patz JA: The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of Falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg. 2006, 74: 3-11.PubMed
50.
go back to reference Chuquiyauri R, Paredes M, Peñataro P, Torres S, Marin S, Tenorio A, Brouwer KC, Abeles S, Llanos-Cuentas A, Gilman RH, Kosek M, Vinetz JM: Socio-demographics and the development of malaria elimination strategies in the low transmission setting. Acta Trop. 2012, 121: 292-302. 10.1016/j.actatropica.2011.11.003.PubMedCentralCrossRefPubMed Chuquiyauri R, Paredes M, Peñataro P, Torres S, Marin S, Tenorio A, Brouwer KC, Abeles S, Llanos-Cuentas A, Gilman RH, Kosek M, Vinetz JM: Socio-demographics and the development of malaria elimination strategies in the low transmission setting. Acta Trop. 2012, 121: 292-302. 10.1016/j.actatropica.2011.11.003.PubMedCentralCrossRefPubMed
51.
go back to reference De Stricker K, Vuust J, Jepsen S, Oeuvray C, Theisen M: Conservation and heterogeneity of the glutamate-rich protein (GLURP) among field isolates and laboratory lines of Plasmodium falciparum. Mol Biochem Parasitol. 2000, 111: 123-130. 10.1016/S0166-6851(00)00304-2.CrossRefPubMed De Stricker K, Vuust J, Jepsen S, Oeuvray C, Theisen M: Conservation and heterogeneity of the glutamate-rich protein (GLURP) among field isolates and laboratory lines of Plasmodium falciparum. Mol Biochem Parasitol. 2000, 111: 123-130. 10.1016/S0166-6851(00)00304-2.CrossRefPubMed
52.
go back to reference Speybroeck N, Praet N, Claes F, Van Hong N, Torres K, Mao S, Van den Eede P, Thi Thinh T, Gamboa D, Sochantha T, Thang ND, Coosemans M, Büscher P, D’Alessandro U, Berkvens D, Erhart A: True versus apparent malaria infection prevalence: the contribution of a Bayesian approach. PLoS One. 2011, 6: e16705-10.1371/journal.pone.0016705.PubMedCentralCrossRefPubMed Speybroeck N, Praet N, Claes F, Van Hong N, Torres K, Mao S, Van den Eede P, Thi Thinh T, Gamboa D, Sochantha T, Thang ND, Coosemans M, Büscher P, D’Alessandro U, Berkvens D, Erhart A: True versus apparent malaria infection prevalence: the contribution of a Bayesian approach. PLoS One. 2011, 6: e16705-10.1371/journal.pone.0016705.PubMedCentralCrossRefPubMed
Metadata
Title
Assessing malaria transmission in a low endemicity area of north-western Peru
Authors
Angel Rosas-Aguirre
Alejandro Llanos-Cuentas
Niko Speybroeck
Jackie Cook
Juan Contreras-Mancilla
Veronica Soto
Dionicia Gamboa
Edwar Pozo
Oscar J Ponce
Mayne O Pereira
Irene S Soares
Michael Theisen
Umberto D’Alessandro
Annette Erhart
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2013
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-12-339

Other articles of this Issue 1/2013

Malaria Journal 1/2013 Go to the issue

Reviewer acknowledgement

Reviewer acknowledgement

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.