- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- Participant demography and test workflow.
- Prevalence of Plasmodium infections in PNGDF and civilian populations.
- Plasmodium species determined by PCR.
- Proportion of SM infections and distribution of parasite densities.
- Parasite density and fever.
- Hemoglobin concentration in LM and SM infections.
- kelch13 Mutations.
- DISCUSSION
- CONCLUSION
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Müller I , Bockarie M , Alpers M , Smith T , 2003. The epidemiology of malaria in Papua New Guinea. Trends Parasitol 19: 253–259.
-
2.
Betuela I , Maraga S , Hetzel MW , Tandrapah T , Sie A , Yala S , Kundi J , Siba P , Reeder JC , Mueller I , 2012. Epidemiology of malaria in the Papua New Guinean highlands. Trop Med Int Health 17: 1181–1191.
-
3.
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4.
Black RH , 1956. The epidemiology of malaria in the southwest Pacific: changes associated with increasing European contact. Oceania 27: 136–142.
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Peters W , Standfast H , 1957. Report on a malaria survey in the Sepik district. Med J Aust 44: 861–868.
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6.
Mehlotra RK , Lorry K , Kastens W , Miller SM , Alpers MP , Bockarie M , Kazura JW , Zimmerman PA , 2000. Random distribution of mixed species malaria infections in Papua New Guinea. Am J Trop Med Hyg 62: 225–231.
-
7.
Hetzel MW , Morris H , Tarongka N , Barnadas C , Pulford J , Makita L , Siba PM , Mueller I , 2015. Prevalence of malaria across Papua New Guinea after initial roll-out of insecticide-treated mosquito nets. Trop Med Int Health 20: 1745–1755.
-
8.
Mueller I , Widmer S , Michel D , Maraga S , McNamara DT , Kiniboro B , Sie A , Smith TA , Zimmerman PA , 2009. High sensitivity detection of Plasmodium species reveals positive correlations between infections of different species, shifts in age distribution and reduced local variation in Papua New Guinea. Malar J 8: 41.
-
9.
Cooper RD , Waterson DG , Frances SP , Beebe NW , Pluess B , Sweeney AW , 2009. Malaria vectors of Papua New Guinea. Int J Parasitol 39: 1495–1501.
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10.
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11.
Spencer M , 1992. The history of malaria control in the southwest Pacific region, with particular reference to Papua New Guinea and the Solomon Islands. P N G Med J 35: 33–66.
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12.
Breinl A , 1915. On the occurrence and prevalence of diseases in British New Guinea. Ann Trop Med Parasitol 9: 285–334.
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14.
Crane G , Gibson D , Verrall J , Barker-Hudson P , Barker-Hudson BE , Charlwood D , Heywood P , 1985. Malaria and tropical splenomegaly syndrome in the Anga of Morobe Province. P N G Med J 28: 27–34.
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15.
Hetzel MWS , Saweri OPM , Kuadima JJ , Smith I , Ura Y , Tandrapah A , Jamea-Maiasa S , Siba PM , Pulford J , 2018. Papua New Guinea Malaria Indicator Survey 2016–2017: Malaria Prevention, Infection, and Treatment. Goroka, Papua New Guinea: Papua New Guinea Institute of Medical Research.
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Koepfli C et al., 2017. Sustained malaria control over an 8-year period in Papua New Guinea: the challenge of low-density asymptomatic Plasmodium infections. J Infect Dis 216: 1434–1443.
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19.
Vinit R et al., 2020. Decreased bioefficacy of long-lasting insecticidal nets and the resurgence of malaria in Papua New Guinea. Nat Commun 11: 3646.
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20.
Burdam FH et al., 2016. Asymptomatic vivax and falciparum parasitaemia with helminth co-infection: major risk factors for anaemia in early life. PLoS One 11: e0160917.
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21.
Pava Z et al., 2016. Submicroscopic and asymptomatic Plasmodium parasitaemia associated with significant risk of anaemia in Papua, Indonesia. PLoS One 11: e0165340.
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22.
Chourasia MK , Raghavendra K , Bhatt RM , Swain DK , Valecha N , Kleinschmidt I , 2017. Burden of asymptomatic malaria among a tribal population in a forested village of central India: a hidden challenge for malaria control in India. Public Health 147: 92–97.
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23.
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Coleman RE , Kumpitak C , Ponlawat A , Maneechai N , Phunkitchar V , Rachapaew N , Zollner G , Sattabongkot J , 2004. Infectivity of asymptomatic Plasmodium-infected human populations to Anopheles dirus mosquitoes in western Thailand. J Med Entomol 41: 201–208.
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Noedl H , Se Y , Schaecher K , Smith BL , Socheat D , Fukuda MM , 2008. Evidence of artemisinin-resistant malaria in western Cambodia. N Engl J Med 359: 2619–2620.
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Dondorp AM et al., 2009. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361: 455–467.
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Miotto O et al., 2020. Emergence of artemisinin-resistant Plasmodium falciparum with kelch13 C580Y mutations on the island of New Guinea. PLoS Pathog 16: e1009133.
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Ariey F et al., 2014. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505: 50–55.
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Phyo AP et al., 2012. Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet 379: 1960–1966.
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Takala-Harrison S et al., 2015. Independent emergence of artemisinin resistance mutations among Plasmodium falciparum in Southeast Asia. J Infect Dis 211: 670–679.
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34.
Chenet SM et al., 2016. Independent emergence of the Plasmodium falciparum Kelch propeller domain mutant allele C580Y in Guyana. J Infect Dis 213: 1472–1475.
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35.
Mathieu LC et al., 2020. Local emergence in Amazonia of Plasmodium falciparum k13 C580Y mutants associated with in vitro artemisinin resistance. eLife 12: e51015.
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36.
Prosser C , Meyer W , Ellis J , Lee R , 2018. Resistance screening and trend analysis of imported falciparum malaria in NSW, Australia (2010–2016). PLoS One 13: e0197369.
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37.
McCallum F , Mond K , Cheng Q , Furuya-Kanamori L , Auliff A , Kaminiel P , Team APHSS , 2023. A health survey revealing prevalence of vector-borne diseases and tuberculosis in Papua New Guinea Defence Force personnel and families. Am J Trop Med Hyg 109: 1086–1094.
-
38.
Padley D , Moody AH , Chiodini PL , Saldanha J , 2003. Use of a rapid, single-round, multiplex PCR to detect malarial parasites and identify the species present. Ann Trop Med Parasitol 97: 131–137.
-
39.
Harris I et al., 2010. 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.
-
40.
Mfuh KO , Achonduh-Atijegbe OA , Bekindaka ON , Esemu LF , Mbakop CD , Gandhi K , Leke RGF , Taylor DW , Nerurkar VR , 2019. A comparison of thick-film microscopy, rapid diagnostic test, and polymerase chain reaction for accurate diagnosis of Plasmodium falciparum malaria. Malar J 18: 73.
-
41.
Wu L , van den Hoogen LL , Slater H , Walker PGT , Ghani AC , Drakeley CJ , Okell LC , 2015. Comparison of diagnostics for the detection of asymptomatic Plasmodium falciparum infections to inform control and elimination strategies. Nature 528: S86–S93.
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Burden of Submicroscopic Plasmodium Infections and Detection of kelch13 Mutant Parasites in Military and Civilian Populations in Papua New Guinea
Paul A. Pickering
Paul A. Pickering
Australian Defence Force Malaria and Infectious Disease Institute, Brisbane, Australia;
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Ivor Harris
Ivor Harris
Australian Defence Force Malaria and Infectious Disease Institute, Brisbane, Australia;
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David Smith
David Smith
Australian Defence Force Malaria and Infectious Disease Institute, Brisbane, Australia;
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Fiona McCallum
Fiona McCallum
Australian Defence Force Malaria and Infectious Disease Institute, Brisbane, Australia;
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Peter Kaminiel
Peter Kaminiel
Papua New Guinea Defence Force Health Service, Port Moresby, Papua New Guinea
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Alyson Auliff
Alyson Auliff
Australian Defence Force Malaria and Infectious Disease Institute, Brisbane, Australia;
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Qin Cheng
Qin Cheng
Australian Defence Force Malaria and Infectious Disease Institute, Brisbane, Australia;
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ABSTRACT.
Malaria remains a major public health problem in Papua New Guinea (PNG) and an important force health protection issue for both PNG and Australian Defence Forces. To investigate the malaria burden in the military and civilians residing on military bases, a cross-sectional survey was conducted in April 2019 at three military bases in Wewak, Manus Island, and Vanimo, PNG. A total of 1,041 participants were enrolled; 235 military personnel from three bases and 806 civilians from Wewak and Vanimo. Polymerase chain reaction (PCR) revealed an overall high prevalence of Plasmodium infection in both the military and civilians. Among the military, the infection prevalence was significantly higher in Wewak (35.5%) and Vanimo (33.3%) bases than on Manus Island (11.8%). Among civilians, children (<16 years old) had significantly higher odds of being PCR positive than adults (≥16 years old). At Wewak and Vanimo, Plasmodium vivax accounted for 85.4%, 78.2%, and 66.2% of infections in military, children, and adult populations. Overall, 87.3%, 41.3%, and 61.3% of Plasmodium infections in the military, children, and adults, respectively, were detected only by PCR, not by microscopy (submicroscopic [SM] infections). Children had a significantly lower proportion of SM infections than adults and Papua New Guinea Defence Force personnel. Infection status was not associated with hemoglobin levels in these populations at the time of the survey. Mutant kelch13 (C580Y) parasites were identified in 5/68 Plasmodium falciparum–infected individuals. The survey results indicate extensive malaria transmission on these bases, especially in Wewak and Vanimo. More intensified interventions are required to reduce malaria transmission on PNG military bases.
Author Notes
Financial support: This work was supported by the
Disclosure: The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of Defence, Australia and the PNG Defence Force. Ethical approvals for the conduct of the survey and laboratory tests were granted by the Departments of Defence and Veterans’ Affairs Human Research Ethics Committee (DDVA HREC 084-18) and the Medical Research Advisory Committee of PNG (MRAC No: 18.21).
Data availability: Data generated from this study are included in the published article or as supplementary information. Data are also available from the corresponding author on request.
Authors’ addresses: Paul A. Pickering, Ivor Harris, David Smith, Fiona McCallum, Alyson Auliff, and Qin Cheng, Australian Defence Force Malaria and Infectious Disease Institute, Brisbane, Australia, E-mails: paul.pickering@defence.gov.au, ivorharris@hotmail.com, david.smith77@defence.gov.au, fiona.mccallum@defence.gov.au, alyson.auliff@defence.gov.au, and qin.cheng@defence.gov.au. Peter Kaminiel, Papua New Guinea Defence Force Health Service, Port Moresby, Papua New Guinea, E-mail: pngdfdhs007@gmail.com.
- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- RESULTS
- Participant demography and test workflow.
- Prevalence of Plasmodium infections in PNGDF and civilian populations.
- Plasmodium species determined by PCR.
- Proportion of SM infections and distribution of parasite densities.
- Parasite density and fever.
- Hemoglobin concentration in LM and SM infections.
- kelch13 Mutations.
- DISCUSSION
- CONCLUSION
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Müller I , Bockarie M , Alpers M , Smith T , 2003. The epidemiology of malaria in Papua New Guinea. Trends Parasitol 19: 253–259.
-
2.
Betuela I , Maraga S , Hetzel MW , Tandrapah T , Sie A , Yala S , Kundi J , Siba P , Reeder JC , Mueller I , 2012. Epidemiology of malaria in the Papua New Guinean highlands. Trop Med Int Health 17: 1181–1191.
-
3.
Ford E , 1950. The malaria problem in Australia and the Australian Pacific territories. Med J Aust 1: 749–760.
-
4.
Black RH , 1956. The epidemiology of malaria in the southwest Pacific: changes associated with increasing European contact. Oceania 27: 136–142.
-
5.
Peters W , Standfast H , 1957. Report on a malaria survey in the Sepik district. Med J Aust 44: 861–868.
-
6.
Mehlotra RK , Lorry K , Kastens W , Miller SM , Alpers MP , Bockarie M , Kazura JW , Zimmerman PA , 2000. Random distribution of mixed species malaria infections in Papua New Guinea. Am J Trop Med Hyg 62: 225–231.
-
7.
Hetzel MW , Morris H , Tarongka N , Barnadas C , Pulford J , Makita L , Siba PM , Mueller I , 2015. Prevalence of malaria across Papua New Guinea after initial roll-out of insecticide-treated mosquito nets. Trop Med Int Health 20: 1745–1755.
-
8.
Mueller I , Widmer S , Michel D , Maraga S , McNamara DT , Kiniboro B , Sie A , Smith TA , Zimmerman PA , 2009. High sensitivity detection of Plasmodium species reveals positive correlations between infections of different species, shifts in age distribution and reduced local variation in Papua New Guinea. Malar J 8: 41.
-
9.
Cooper RD , Waterson DG , Frances SP , Beebe NW , Pluess B , Sweeney AW , 2009. Malaria vectors of Papua New Guinea. Int J Parasitol 39: 1495–1501.
-
10.
Black RH , 1955. Malaria in the South-West Pacific. Noumea, New Caledonia: South Pacific Commission.
-
11.
Spencer M , 1992. The history of malaria control in the southwest Pacific region, with particular reference to Papua New Guinea and the Solomon Islands. P N G Med J 35: 33–66.
-
12.
Breinl A , 1915. On the occurrence and prevalence of diseases in British New Guinea. Ann Trop Med Parasitol 9: 285–334.
-
13.
Parkinson A , 1974. Malaria in Papua New Guinea 1973. P N G Med J 17: 8–16.
-
14.
Crane G , Gibson D , Verrall J , Barker-Hudson P , Barker-Hudson BE , Charlwood D , Heywood P , 1985. Malaria and tropical splenomegaly syndrome in the Anga of Morobe Province. P N G Med J 28: 27–34.
-
15.
Hetzel MWS , Saweri OPM , Kuadima JJ , Smith I , Ura Y , Tandrapah A , Jamea-Maiasa S , Siba PM , Pulford J , 2018. Papua New Guinea Malaria Indicator Survey 2016–2017: Malaria Prevention, Infection, and Treatment. Goroka, Papua New Guinea: Papua New Guinea Institute of Medical Research.
-
16.
Hetzel MW et al., 2017. Insecticide-treated nets and malaria prevalence, Papua New Guinea, 2008–2014. Bull World Health Organ 95: 695–705B.
-
17.
WHO , 2022. World Malaria Report 2022. Geneva, Switzerland: World Health Organization.
-
18.
Koepfli C et al., 2017. Sustained malaria control over an 8-year period in Papua New Guinea: the challenge of low-density asymptomatic Plasmodium infections. J Infect Dis 216: 1434–1443.
-
19.
Vinit R et al., 2020. Decreased bioefficacy of long-lasting insecticidal nets and the resurgence of malaria in Papua New Guinea. Nat Commun 11: 3646.
-
20.
Burdam FH et al., 2016. Asymptomatic vivax and falciparum parasitaemia with helminth co-infection: major risk factors for anaemia in early life. PLoS One 11: e0160917.
-
21.
Pava Z et al., 2016. Submicroscopic and asymptomatic Plasmodium parasitaemia associated with significant risk of anaemia in Papua, Indonesia. PLoS One 11: e0165340.
-
22.
Chourasia MK , Raghavendra K , Bhatt RM , Swain DK , Valecha N , Kleinschmidt I , 2017. Burden of asymptomatic malaria among a tribal population in a forested village of central India: a hidden challenge for malaria control in India. Public Health 147: 92–97.
-
23.
Sharma V , Choudhury D , Ansari M , Malhotra M , Menon P , Razdan R , Batra C , 1983. Studies on the true incidence of malaria in Kharkhoda (district Sonepat, Haryana) and Kichha (district Nainital, UP) primary health centres. Indian J Malariol 20: 21–34.
-
24.
Okell LC , Ghani AC , Lyons E , Drakeley CJ , 2009. Submicroscopic infection in Plasmodium falciparum–endemic populations: a systematic review and meta-analysis. J Infect Dis 200: 1509–1517.
-
25.
Cheng Q , Cunningham J , Gatton ML , 2015. Systematic review of sub-microscopic P. vivax infections: prevalence and determining factors. PLoS Negl Trop Dis 9: e3413.
-
26.
Nwakanma D , Kheir A , Sowa M , Dunyo S , Jawara M , Pinder M , Milligan P , Walliker D , Babiker HA , 2008. High gametocyte complexity and mosquito infectivity of Plasmodium falciparum in the Gambia. Int J Parasitol 38: 219–227.
-
27.
Coleman RE , Kumpitak C , Ponlawat A , Maneechai N , Phunkitchar V , Rachapaew N , Zollner G , Sattabongkot J , 2004. Infectivity of asymptomatic Plasmodium-infected human populations to Anopheles dirus mosquitoes in western Thailand. J Med Entomol 41: 201–208.
-
28.
Noedl H , Se Y , Schaecher K , Smith BL , Socheat D , Fukuda MM , 2008. Evidence of artemisinin-resistant malaria in western Cambodia. N Engl J Med 359: 2619–2620.
-
29.
Dondorp AM et al., 2009. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361: 455–467.
-
30.
Miotto O et al., 2020. Emergence of artemisinin-resistant Plasmodium falciparum with kelch13 C580Y mutations on the island of New Guinea. PLoS Pathog 16: e1009133.
-
31.
Ariey F et al., 2014. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505: 50–55.
-
32.
Phyo AP et al., 2012. Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet 379: 1960–1966.
-
33.
Takala-Harrison S et al., 2015. Independent emergence of artemisinin resistance mutations among Plasmodium falciparum in Southeast Asia. J Infect Dis 211: 670–679.
-
34.
Chenet SM et al., 2016. Independent emergence of the Plasmodium falciparum Kelch propeller domain mutant allele C580Y in Guyana. J Infect Dis 213: 1472–1475.
-
35.
Mathieu LC et al., 2020. Local emergence in Amazonia of Plasmodium falciparum k13 C580Y mutants associated with in vitro artemisinin resistance. eLife 12: e51015.
-
36.
Prosser C , Meyer W , Ellis J , Lee R , 2018. Resistance screening and trend analysis of imported falciparum malaria in NSW, Australia (2010–2016). PLoS One 13: e0197369.
-
37.
McCallum F , Mond K , Cheng Q , Furuya-Kanamori L , Auliff A , Kaminiel P , Team APHSS , 2023. A health survey revealing prevalence of vector-borne diseases and tuberculosis in Papua New Guinea Defence Force personnel and families. Am J Trop Med Hyg 109: 1086–1094.
-
38.
Padley D , Moody AH , Chiodini PL , Saldanha J , 2003. Use of a rapid, single-round, multiplex PCR to detect malarial parasites and identify the species present. Ann Trop Med Parasitol 97: 131–137.
-
39.
Harris I et al., 2010. 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.
-
40.
Mfuh KO , Achonduh-Atijegbe OA , Bekindaka ON , Esemu LF , Mbakop CD , Gandhi K , Leke RGF , Taylor DW , Nerurkar VR , 2019. A comparison of thick-film microscopy, rapid diagnostic test, and polymerase chain reaction for accurate diagnosis of Plasmodium falciparum malaria. Malar J 18: 73.
-
41.
Wu L , van den Hoogen LL , Slater H , Walker PGT , Ghani AC , Drakeley CJ , Okell LC , 2015. Comparison of diagnostics for the detection of asymptomatic Plasmodium falciparum infections to inform control and elimination strategies. Nature 528: S86–S93.
-
42.
Genton B , al-Yaman F , Beck HP , Hii J , Mellor S , Narara A , Gibson N , Smith T , Alpers MP , 1995. The epidemiology of malaria in the Wosera area, East Sepik Province, Papua New Guinea, in preparation for vaccine trials. I. Malariometric indices and immunity. Ann Trop Med Parasitol 89: 359–376.
-
43.
Kattenberg JH et al., 2020. The epidemiology of Plasmodium falciparum and Plasmodium vivax in East Sepik Province, Papua New Guinea, pre- and post-implementation of national malaria control efforts. Malar J 19: 198.
-
44.
Okell LC , Bousema T , Griffin JT , Ouédraogo AL , Ghani AC , Drakeley CJ , 2012. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun 3: 1237.
-
45.
Sattabongkot J , Maneechai N , Phunkitchar V , Eikarat N , Khuntirat B , Sirichaisinthop J , Burge R , Coleman RE , 2003. Comparison of artificial membrane feeding with direct skin feeding to estimate the infectiousness of Plasmodium vivax gametocyte carriers to mosquitoes. Am J Trop Med Hyg 69: 529–535.
-
46.
Surit T , Sripoorote P , Kumpitak C , Suansomjit C , Maneechai N , Cui L , Sattabongkot J , Roobsoong W , Nguitragool W , 2023. Transmission efficiency of Plasmodium vivax at low parasitaemia. Malar J 22: 22.
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