The prevalence and density of asymptomatic Plasmodium falciparum infections among children and adults in three communities of western Kenya

Abstract Background Further reductions in malaria incidence as more countries approach malaria elimination require the identification and treatment of asymptomatic individuals who carry mosquito-infective Plasmodium gametocytes that are responsible for furthering malaria transmission. Assessing the...

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Main Authors: Christina Salgado, George Ayodo, Michael D. Macklin, Meetha P. Gould, Srinivas Nallandhighal, Eliud O. Odhiambo, Andrew Obala, Wendy Prudhomme O’Meara, Chandy C. John, Tuan M. Tran
Format: Article
Language:English
Published: BMC 2021-09-01
Series:Malaria Journal
Subjects:
Online Access:https://doi.org/10.1186/s12936-021-03905-w
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language English
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author Christina Salgado
George Ayodo
Michael D. Macklin
Meetha P. Gould
Srinivas Nallandhighal
Eliud O. Odhiambo
Andrew Obala
Wendy Prudhomme O’Meara
Chandy C. John
Tuan M. Tran
spellingShingle Christina Salgado
George Ayodo
Michael D. Macklin
Meetha P. Gould
Srinivas Nallandhighal
Eliud O. Odhiambo
Andrew Obala
Wendy Prudhomme O’Meara
Chandy C. John
Tuan M. Tran
The prevalence and density of asymptomatic Plasmodium falciparum infections among children and adults in three communities of western Kenya
Malaria Journal
Malaria
Plasmodium falciparum
Asymptomatic infection
Gametocytes
PIESP2
Cross-sectional study
author_facet Christina Salgado
George Ayodo
Michael D. Macklin
Meetha P. Gould
Srinivas Nallandhighal
Eliud O. Odhiambo
Andrew Obala
Wendy Prudhomme O’Meara
Chandy C. John
Tuan M. Tran
author_sort Christina Salgado
title The prevalence and density of asymptomatic Plasmodium falciparum infections among children and adults in three communities of western Kenya
title_short The prevalence and density of asymptomatic Plasmodium falciparum infections among children and adults in three communities of western Kenya
title_full The prevalence and density of asymptomatic Plasmodium falciparum infections among children and adults in three communities of western Kenya
title_fullStr The prevalence and density of asymptomatic Plasmodium falciparum infections among children and adults in three communities of western Kenya
title_full_unstemmed The prevalence and density of asymptomatic Plasmodium falciparum infections among children and adults in three communities of western Kenya
title_sort prevalence and density of asymptomatic plasmodium falciparum infections among children and adults in three communities of western kenya
publisher BMC
series Malaria Journal
issn 1475-2875
publishDate 2021-09-01
description Abstract Background Further reductions in malaria incidence as more countries approach malaria elimination require the identification and treatment of asymptomatic individuals who carry mosquito-infective Plasmodium gametocytes that are responsible for furthering malaria transmission. Assessing the relationship between total parasitaemia and gametocytaemia in field surveys can provide insight as to whether detection of low-density, asymptomatic Plasmodium falciparum infections with sensitive molecular methods can adequately detect the majority of infected individuals who are potentially capable of onward transmission. Methods In a cross-sectional survey of 1354 healthy children and adults in three communities in western Kenya across a gradient of malaria transmission (Ajigo, Webuye, and Kapsisywa–Kipsamoite), asymptomatic P. falciparum infections were screened by rapid diagnostic tests, blood smear, and quantitative PCR of dried blood spots targeting the varATS gene in genomic DNA. A multiplex quantitative reverse-transcriptase PCR assay targeting female and male gametocyte genes (pfs25, pfs230p), a gene with a transcriptional pattern restricted to asexual blood stages (piesp2), and human GAPDH was also developed to determine total parasite and gametocyte densities among parasitaemic individuals. Results The prevalence of varATS-detectable asymptomatic infections was greatest in Ajigo (42%), followed by Webuye (10%). Only two infections were detected in Kapsisywa. No infections were detected in Kipsamoite. Across all communities, children aged 11–15 years account for the greatest proportion total and sub-microscopic asymptomatic infections. In younger age groups, the majority of infections were detectable by microscopy, while 68% of asymptomatically infected adults (> 21 years old) had sub-microscopic parasitaemia. Piesp2-derived parasite densities correlated poorly with microscopy-determined parasite densities in patent infections relative to varATS-based detection. In general, both male and female gametocytaemia increased with increasing varATS-derived total parasitaemia. A substantial proportion (41.7%) of individuals with potential for onward transmission had qPCR-estimated parasite densities below the limit of microscopic detection, but above the detectable limit of varATS qPCR. Conclusions This assessment of parasitaemia and gametocytaemia in three communities with different transmission intensities revealed evidence of a substantial sub-patent infectious reservoir among asymptomatic carriers of P. falciparum. Experimental studies are needed to definitively determine whether the low-density infections in communities such as Ajigo and Webuye contribute significantly to malaria transmission.
topic Malaria
Plasmodium falciparum
Asymptomatic infection
Gametocytes
PIESP2
Cross-sectional study
url https://doi.org/10.1186/s12936-021-03905-w
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spelling doaj-5f9b8352e785465b8dd1ebfda8abf1272021-09-19T11:47:56ZengBMCMalaria Journal1475-28752021-09-0120111110.1186/s12936-021-03905-wThe prevalence and density of asymptomatic Plasmodium falciparum infections among children and adults in three communities of western KenyaChristina Salgado0George Ayodo1Michael D. Macklin2Meetha P. Gould3Srinivas Nallandhighal4Eliud O. Odhiambo5Andrew Obala6Wendy Prudhomme O’Meara7Chandy C. John8Tuan M. Tran9Division of Infectious Diseases, Department of Medicine, Indiana University School of MedicineCenter for Global Health Research, Kenya Medical Research InstituteDivision of Infectious Diseases, Department of Medicine, Indiana University School of MedicineReserve Analytics, LLPDivision of Infectious Diseases, Department of Medicine, Indiana University School of MedicineRyan White Center for Pediatric Infectious Diseases and Global Health, Department of Pediatrics, Indiana University School of MedicineSchool of Medicine, Moi University College of Health SciencesDuke Global Health Institute, Duke UniversityRyan White Center for Pediatric Infectious Diseases and Global Health, Department of Pediatrics, Indiana University School of MedicineDivision of Infectious Diseases, Department of Medicine, Indiana University School of MedicineAbstract Background Further reductions in malaria incidence as more countries approach malaria elimination require the identification and treatment of asymptomatic individuals who carry mosquito-infective Plasmodium gametocytes that are responsible for furthering malaria transmission. Assessing the relationship between total parasitaemia and gametocytaemia in field surveys can provide insight as to whether detection of low-density, asymptomatic Plasmodium falciparum infections with sensitive molecular methods can adequately detect the majority of infected individuals who are potentially capable of onward transmission. Methods In a cross-sectional survey of 1354 healthy children and adults in three communities in western Kenya across a gradient of malaria transmission (Ajigo, Webuye, and Kapsisywa–Kipsamoite), asymptomatic P. falciparum infections were screened by rapid diagnostic tests, blood smear, and quantitative PCR of dried blood spots targeting the varATS gene in genomic DNA. A multiplex quantitative reverse-transcriptase PCR assay targeting female and male gametocyte genes (pfs25, pfs230p), a gene with a transcriptional pattern restricted to asexual blood stages (piesp2), and human GAPDH was also developed to determine total parasite and gametocyte densities among parasitaemic individuals. Results The prevalence of varATS-detectable asymptomatic infections was greatest in Ajigo (42%), followed by Webuye (10%). Only two infections were detected in Kapsisywa. No infections were detected in Kipsamoite. Across all communities, children aged 11–15 years account for the greatest proportion total and sub-microscopic asymptomatic infections. In younger age groups, the majority of infections were detectable by microscopy, while 68% of asymptomatically infected adults (> 21 years old) had sub-microscopic parasitaemia. Piesp2-derived parasite densities correlated poorly with microscopy-determined parasite densities in patent infections relative to varATS-based detection. In general, both male and female gametocytaemia increased with increasing varATS-derived total parasitaemia. A substantial proportion (41.7%) of individuals with potential for onward transmission had qPCR-estimated parasite densities below the limit of microscopic detection, but above the detectable limit of varATS qPCR. Conclusions This assessment of parasitaemia and gametocytaemia in three communities with different transmission intensities revealed evidence of a substantial sub-patent infectious reservoir among asymptomatic carriers of P. falciparum. Experimental studies are needed to definitively determine whether the low-density infections in communities such as Ajigo and Webuye contribute significantly to malaria transmission.https://doi.org/10.1186/s12936-021-03905-wMalariaPlasmodium falciparumAsymptomatic infectionGametocytesPIESP2Cross-sectional study