- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- Study design and areas.
- Study population and sample size.
- Data collection, blood collection, and DNA extraction.
- Protocol used to determinate pfhrp2/3 deletions.
- Molecular detection of P. falciparum infections with parasitemia >100 parasites/µL.
- Amplification of pfhrp2 and pfhrp3 genes.
- Control quality of the specificity of pfhrp2/3 primers.
- Assessing of DNA quality and clonality of infections with pfhrp2/3 deletions.
- Operational definitions.
- STATISTICAL ANALYSES
- RESULTS
- Sociodemographic and clinical characteristics of samples.
- Quantitative real-time PCR standardization results.
- Proportion of pfhrp2 and pfhrp3 gene deletions.
- Clonality of infections in samples with pfhrp2/3 deletions.
- Profile of pfhrp2/3 deletions by geographic area, gender, age, asymptomatic, and submicroscopic infections.
- DISCUSSION
- CONCLUSION
- Supplemental Materials
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization , 2023. World Malaria Report 2023. Geneva, Switzerland: WHO.
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White NJ , Pukrittayakamee S , Tinh Hien T , Abul Faiz M , Mokuolu OA , Dondorp AM , 2014. Malaria. Lancet 391: 1608–1621.
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Moody A , 2002. Rapid diagnostic tests for malaria parasites. Clin Microbiol Rev 15: 66–78.
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Gamboa D et al., 2010. A large proportion of P. falciparum isolates in the Amazon region of Peru lack pfhrp2 and pfhrp3: Implications for malaria rapid diagnostic tests. PLoS One 5: e8091.
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Kojom LP , Singh V , 2020. Prevalence of Plasmodium falciparum field isolates with deletions in histidine-rich protein 2 and 3 genes in context with sub-Saharan Africa and India: A systematic review and meta-analysis. Malar J 19: 46.
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Eyong EM , Etutu Molua SJ , Fru-Cho J , Nyasa RB , Kwenti Tebit E , Moyeh MN , 2022. Plasmodium falciparum histidine-rich Protein 2 (pfhrp2) and histidine-rich protein 3 (pfhrp3) genes deletion in the Mount Cameroon region. IJID Reg 3: 300–307.
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13.
Dongang Nana RR , Ngum LN , Makoge V , Adja Amvongo N , Hawadak J , Singh V , 2024. Rapid diagnostic tests for malaria diagnosis in Cameroon: Impact of histidine rich protein 2/3 deletions and lactate dehydrogenase gene polymorphism. Diagn Microbiol Infect Dis 108: 116103.
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Kumar N , Pande V , Bhatt RM , Shah NK , Mishra N , Srivastava B , Valecha N , Anvikar AR , 2013. Genetic deletion of HRP2 and HRP3 in Indian Plasmodium falciparum population and false negative malaria rapid diagnostic test. Acta Trop 125: 119–121.
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Bharti PK , Chandel HS , Ahmad A , Krishna S , Udhayakumar V , Singh N , 2016. Prevalence of pfhrp2 and/or pfhrp3 gene deletion in Plasmodium falciparum population in eight highly endemic states in India. PLoS One 11: e0157949.
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Pati P , Dhangadamajhi G , Bal M , Ranjit M , 2018. High proportions of pfhrp2 gene deletion and performance of HRP2–based rapid diagnostic test in Plasmodium falciparum field isolates of Odisha. Malar J 17: 394.
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Acharya A , Saha P , Chaudhury A , Guha SK , Maji AK , 2023. Prevalence of histidine-rich protein 2 deletion among the Plasmodium falciparum isolates from Kolkata. Trop Parasitol 13: 16–21.
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Kumari S , Ahmed M , Sharma S , Pande V , Anvikar A , 2021. Prevalence of Pfhrp2/3 gene deletions among false negative rapid antigen test results in central India. J Vector Borne Dis 58: 273–280.
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Kumari MS , Sharma S , Bhardwaj N , Kumar S , Ahmed MZ , Pande V , Anvikar AR , 2022. Pfhrp2/3 gene deletion and genetic variation in PfHRP2-based RDTs with P. falciparum positive samples from India and its implication on malaria control. Infect Genet Evol 99: 105232.
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Sivaradjy M , Hamide A , Krishnamoorthy S , Rajkumari N , Mohan V , Sharmila FM , 2022. Assessment of Plasmodium falciparum histidine rich protein 2 and/3 (pfhrp2 &/pfhrp3) gene deletion or mutation in Plasmodium falciparum positive blood samples in a tertiary care centre in south India. J Parasit Dis 46: 729–743.
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Kojom Foko LP , Hawadak J , Kouemo Motse FD , Eboumbou Moukoko EC , Kamgain Mawabo L , Pande V , Singh V , 2022. Non-falciparum species and submicroscopic infections in three epidemiological malaria facets in Cameroon. BMC Infect Dis 22: 900.
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Antonio-Nkondjio C , Ndo C , Njiokou F , Bigoga JD , Awono-Ambene P , Etang J , Ekobo AS , Wondji CS , 2019. Review of malaria situation in Cameroon: Technical viewpoint on challenges and prospects for disease elimination. Parasit Vectors 12: 501.
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Khan N , Awasthi G , Das A , 2023. How can the complex epidemiology of malaria in India impact its elimination? Trends Parasitol 39: 432–444.
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Parr JB , Anderson O , Juliano JJ , Meshnick SR , 2018. Streamlined, PCR-based testing for pfhrp2- and pfhrp3-negative Plasmodium falciparum. Malar J 17: 137.
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Bauffe F , Desplans J , Fraisier C , Parzy D , 2012. Real-time PCR assay for discrimination of Plasmodium ovale curtisi and Plasmodium ovale wallikeri in the Ivory Coast and in the Comoros Islands. Malar J 11: 307.
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Reed GF , Lynn F , Meade BD , 2002. Use of coefficient of variation in assessing variability of quantitative assays. Clin Diagn Lab Immunol 9: 1235–1239.
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Snounou G , Zhu X , Siripoon N , Jarra W , Thaithong S , Brown KN , Viriyakosol S , 1999. Biased distribution of msp1 and msp2 allelic variants in Plasmodium falciparum populations in Thailand. Trans R Soc Trop Med Hyg 93: 369–374.
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Deletions of Histidine-Rich Protein 2/3 Genes in Natural Plasmodium falciparum Populations from Cameroon and India: Role of Asymptomatic and Submicroscopic Infections
Loick Pradel Kojom Foko
Loick Pradel Kojom Foko
National Institute of Malaria Research, New Delhi, India;
Department of Biotechnology, Kumaun University, Bhimtal, India;
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Department of Biotechnology, Kumaun University, Bhimtal, India;
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Carole Else Eboumbou Moukoko
Carole Else Eboumbou Moukoko
Department of Biological Sciences, Faculty of Medicine and Pharmaceutical Sciences, The University of Douala, Douala, Cameroon;
Malaria Research Unit, Centre Pasteur Cameroon, Yaoundé, Cameroon;
Laboratory of Parasitology, Mycology and Virology, Postgraduate Training Unit for Health Sciences, Postgraduate School for Pure and Applied Sciences, The University of Douala, Douala, Cameroon;
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Malaria Research Unit, Centre Pasteur Cameroon, Yaoundé, Cameroon;
Laboratory of Parasitology, Mycology and Virology, Postgraduate Training Unit for Health Sciences, Postgraduate School for Pure and Applied Sciences, The University of Douala, Douala, Cameroon;
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Jahnvi Jakhan
Jahnvi Jakhan
National Institute of Malaria Research, New Delhi, India;
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Geetika Narang
Geetika Narang
National Institute of Malaria Research, New Delhi, India;
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Joseph Hawadak
Joseph Hawadak
National Institute of Malaria Research, New Delhi, India;
Department of Biotechnology, Kumaun University, Bhimtal, India;
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Department of Biotechnology, Kumaun University, Bhimtal, India;
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Francine Dorgelesse Kouemo Motse
Francine Dorgelesse Kouemo Motse
Department of Medical Laboratory Sciences, Faculty of Health Sciences, University of Buea, Buea, Cameroon,
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Veena Pande
Veena Pande
Department of Biotechnology, Kumaun University, Bhimtal, India;
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Vineeta Singh
Vineeta Singh
National Institute of Malaria Research, New Delhi, India;
Academy of Scientific and Innovative Research, Ghaziabad, India
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Academy of Scientific and Innovative Research, Ghaziabad, India
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ABSTRACT.
The bulk of malaria rapid diagnostic tests (RDTs) target histidine-rich protein 2 of Plasmodium falciparum, the deadliest malaria species. The WHO considers pfhrp2/3 deletions as one of the main threats to successful malaria control and/or elimination; as such, parasites that lack part or all of the pfhrp2 gene are missed by pfHRP2-targeting RDTs. Such deletions have been reported in several African and Asian countries, but little is known in Cameroon and India. Blood samples were collected from individuals living in four areas of Cameroon (Douala, Maroua, Mayo-Oulo, Pette) and India (Mewat, Raipur, Ranchi, Rourkela). Deletions in pfhrp2/3 genes were confirmed if samples 1) had ≥100 parasites/µL by quantitative polymerase chain reaction (PCR), 2) PCR negative for pfhrp2/3, and 3) PCR positive for at least two single-copy genes. The overall proportion of pfhrp2 and pfhrp3 deletions in Cameroon was 13.5% and 3.1%. In India, the overall proportion was 8% for pfhrp2 and 4% for pfhrp3. The overall proportions of samples with both gene deletions (pfhrp2–/3–) were 3.1% in Cameroon and 1.3% in India. In Cameroon, pfhrp2–/3+ and pfhrp2–/3– deletions were common in Maroua (P = 0.02), in asymptomatic parasitemia (P = 0.006) and submicroscopic parasitemia (P <0.0001). In both countries, pfhrp2/3 deletions, including pfhrp2–/3– deletions, were mainly seen in monoclonal infections. This study outlines that double deletions that result in false negative RDTs are uncommon in our settings, and highlights the importance of active molecular surveillance for pfhrp2/3 deletions in Cameroon and India.
- Supplemental Materials (PDF 1035.9 KB)
Author Notes
Author’s addresses: Loick Pradel Kojom Foko and Joseph Hawadak, National Institute of Malaria Research, New Delhi, India, and Department of Biotechnology, Kumaun University, Bhimtal, India. E-mails: kojomloick@gmail.com and johawadak@yahoo.fr. Carole Else Eboumbou Moukoko, Department of Biological Sciences, Faculty of Medicine and Pharmaceutical Sciences, The University of Douala, Douala, Cameroon, Malaria Research Unit, Centre Pasteur Cameroon, Yaoundé, Cameroon, and Laboratory of Parasitology, Mycology and Virology, Postgraduate Training Unit for Health Sciences, Postgraduate School for Pure and Applied Sciences, The University of Douala, Douala, Cameroon, E-mail: elsecarole@yahoo.fr. Jahnvi Jakhan and Geetika Narang, National Institute of Malaria Research, New Delhi, India, E-mails: dr.jahnvijakhan@gmail.com and narang1geetika@gmail.com. Francine Dorgelesse Kouemo Motse, Department of Medical Laboratory Sciences, Faculty of Health Sciences, University of Buea, Buea, Cameroon, E-mail: kouemofrancine@yahoo.fr. Veena Pande, Department of Biotechnology, Kumaun University, Bhimtal, India, E-mail: veena.biotech@gmail.com. Vineeta Singh, National Institute of Malaria Research, New Delhi, India, and Academy of Scientific and Innovative Research, Ghaziabad, India, E-mail: vineetas_2000@yahoo.com.
- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- Study design and areas.
- Study population and sample size.
- Data collection, blood collection, and DNA extraction.
- Protocol used to determinate pfhrp2/3 deletions.
- Molecular detection of P. falciparum infections with parasitemia >100 parasites/µL.
- Amplification of pfhrp2 and pfhrp3 genes.
- Control quality of the specificity of pfhrp2/3 primers.
- Assessing of DNA quality and clonality of infections with pfhrp2/3 deletions.
- Operational definitions.
- STATISTICAL ANALYSES
- RESULTS
- Sociodemographic and clinical characteristics of samples.
- Quantitative real-time PCR standardization results.
- Proportion of pfhrp2 and pfhrp3 gene deletions.
- Clonality of infections in samples with pfhrp2/3 deletions.
- Profile of pfhrp2/3 deletions by geographic area, gender, age, asymptomatic, and submicroscopic infections.
- DISCUSSION
- CONCLUSION
- Supplemental Materials
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization , 2023. World Malaria Report 2023. Geneva, Switzerland: WHO.
-
2.
White NJ , Pukrittayakamee S , Tinh Hien T , Abul Faiz M , Mokuolu OA , Dondorp AM , 2014. Malaria. Lancet 391: 1608–1621.
-
3.
Wongsrichanalai C , Barcus MJ , Muth S , Sutamihardja A , Wernsdorfer WH , 2007. A review of malaria diagnostic tools: Microscopy and rapid diagnostic test (RDT). Am J Trop Med Hyg 77: 119–127.
-
4.
Moody A , 2002. Rapid diagnostic tests for malaria parasites. Clin Microbiol Rev 15: 66–78.
-
5.
Kojom Foko LP , Pande V , Singh V , 2021. Field performances of rapid diagnostic tests detecting human Plasmodium species: A systematic review and meta-analysis in India, 1990–2020. Diagnostics (Basel) 11: 590.
-
6.
World Health Organization , 2018. World Malaria Report 2018. Geneva, Switzerland: WHO.
-
7.
Thomson R , Beshir KB , Cunningham J , Baiden F , Bharmal J , Bruxvoort KJ , Maiteki-Sebuguzi C , Owusu-Agyei S , Staedke SG , Hopkins H , 2019. pfhrp2 and pfhrp3 gene deletions that affect malaria rapid diagnostic tests for Plasmodium falciparum: Analysis of archived blood samples from three African countries. J Infect Dis 220: 1444–1452.
-
8.
Gamboa D et al., 2010. A large proportion of P. falciparum isolates in the Amazon region of Peru lack pfhrp2 and pfhrp3: Implications for malaria rapid diagnostic tests. PLoS One 5: e8091.
-
9.
Kojom LP , Singh V , 2020. Prevalence of Plasmodium falciparum field isolates with deletions in histidine-rich protein 2 and 3 genes in context with sub-Saharan Africa and India: A systematic review and meta-analysis. Malar J 19: 46.
-
10.
World Health Organization , 2022. World Malaria Report 2022. Geneva, Switzerland: WHO.
-
11.
World Health Organization , 2018. High Burden to High Impact: A Targeted Malaria Response. Geneva, Switzerland: WHO.
-
12.
Eyong EM , Etutu Molua SJ , Fru-Cho J , Nyasa RB , Kwenti Tebit E , Moyeh MN , 2022. Plasmodium falciparum histidine-rich Protein 2 (pfhrp2) and histidine-rich protein 3 (pfhrp3) genes deletion in the Mount Cameroon region. IJID Reg 3: 300–307.
-
13.
Dongang Nana RR , Ngum LN , Makoge V , Adja Amvongo N , Hawadak J , Singh V , 2024. Rapid diagnostic tests for malaria diagnosis in Cameroon: Impact of histidine rich protein 2/3 deletions and lactate dehydrogenase gene polymorphism. Diagn Microbiol Infect Dis 108: 116103.
-
14.
Kumar N , Pande V , Bhatt RM , Shah NK , Mishra N , Srivastava B , Valecha N , Anvikar AR , 2013. Genetic deletion of HRP2 and HRP3 in Indian Plasmodium falciparum population and false negative malaria rapid diagnostic test. Acta Trop 125: 119–121.
-
15.
Bharti PK , Chandel HS , Ahmad A , Krishna S , Udhayakumar V , Singh N , 2016. Prevalence of pfhrp2 and/or pfhrp3 gene deletion in Plasmodium falciparum population in eight highly endemic states in India. PLoS One 11: e0157949.
-
16.
Pati P , Dhangadamajhi G , Bal M , Ranjit M , 2018. High proportions of pfhrp2 gene deletion and performance of HRP2–based rapid diagnostic test in Plasmodium falciparum field isolates of Odisha. Malar J 17: 394.
-
17.
Acharya A , Saha P , Chaudhury A , Guha SK , Maji AK , 2023. Prevalence of histidine-rich protein 2 deletion among the Plasmodium falciparum isolates from Kolkata. Trop Parasitol 13: 16–21.
-
18.
Kumari S , Ahmed M , Sharma S , Pande V , Anvikar A , 2021. Prevalence of Pfhrp2/3 gene deletions among false negative rapid antigen test results in central India. J Vector Borne Dis 58: 273–280.
-
19.
Kumari MS , Sharma S , Bhardwaj N , Kumar S , Ahmed MZ , Pande V , Anvikar AR , 2022. Pfhrp2/3 gene deletion and genetic variation in PfHRP2-based RDTs with P. falciparum positive samples from India and its implication on malaria control. Infect Genet Evol 99: 105232.
-
20.
Sivaradjy M , Hamide A , Krishnamoorthy S , Rajkumari N , Mohan V , Sharmila FM , 2022. Assessment of Plasmodium falciparum histidine rich protein 2 and/3 (pfhrp2 &/pfhrp3) gene deletion or mutation in Plasmodium falciparum positive blood samples in a tertiary care centre in south India. J Parasit Dis 46: 729–743.
-
21.
Kojom Foko LP , Hawadak J , Kouemo Motse FD , Eboumbou Moukoko EC , Kamgain Mawabo L , Pande V , Singh V , 2022. Non-falciparum species and submicroscopic infections in three epidemiological malaria facets in Cameroon. BMC Infect Dis 22: 900.
-
22.
Antonio-Nkondjio C , Ndo C , Njiokou F , Bigoga JD , Awono-Ambene P , Etang J , Ekobo AS , Wondji CS , 2019. Review of malaria situation in Cameroon: Technical viewpoint on challenges and prospects for disease elimination. Parasit Vectors 12: 501.
-
23.
Khan N , Awasthi G , Das A , 2023. How can the complex epidemiology of malaria in India impact its elimination? Trends Parasitol 39: 432–444.
-
24.
World Health Organization , 2017. Meeting Report of the WHO Evidence Review Group on Low-Density Malaria Infections. Geneva, Switzerland: WHO.
-
25.
Parr JB , Anderson O , Juliano JJ , Meshnick SR , 2018. Streamlined, PCR-based testing for pfhrp2- and pfhrp3-negative Plasmodium falciparum. Malar J 17: 137.
-
26.
Bauffe F , Desplans J , Fraisier C , Parzy D , 2012. Real-time PCR assay for discrimination of Plasmodium ovale curtisi and Plasmodium ovale wallikeri in the Ivory Coast and in the Comoros Islands. Malar J 11: 307.
-
27.
Reed GF , Lynn F , Meade BD , 2002. Use of coefficient of variation in assessing variability of quantitative assays. Clin Diagn Lab Immunol 9: 1235–1239.
-
28.
Ye J , Coulouris G , Zaretskaya I , Cutcutache I , Rozen S , Madden TL , 2012. Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13: 134.
-
29.
Snounou G , Zhu X , Siripoon N , Jarra W , Thaithong S , Brown KN , Viriyakosol S , 1999. Biased distribution of msp1 and msp2 allelic variants in Plasmodium falciparum populations in Thailand. Trans R Soc Trop Med Hyg 93: 369–374.
-
30.
Ménard D et al., 2016. A worldwide map of Plasmodium falciparum K13-Propeller polymorphisms. N Engl J Med 374: 2453–2464.
-
31.
Snounou G , Beck HP , 1998. The use of PCR genotyping in the assessment of recrudescence or reinfection after antimalarial drug treatment. Parasitol Today 14: 462–467.
-
32.
Kamgain L , Assam-Assam J-P , Kojom Foko LP , Fouamno H , 2017. Prevalence of malaria infection and reliability of ACCUCARE One Step Malaria Test® for diagnosing malaria in people living with human immunodeficiency virus infection in Cameroon. Int J Trop Dis Health 21: 1–10.
-
33.
Apinjoh TO et al., 2015. Plasmodium falciparum merozoite surface protein 1 block 2 gene polymorphism in field isolates along the slope of mount Cameroon: A cross-sectional study. BMC Infect Dis 15: 309.
-
34.
Funwei R , Nderu D , Nguetse CN , Thomas BN , Falade CO , Velavan TP , Ojurongbe O , 2019. Molecular surveillance of pfhrp2 and pfhrp3 genes deletion in Plasmodium falciparum isolates and the implications for rapid diagnostic tests in Nigeria. Acta Trop 196: 121–125.
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