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Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Malaria | Research

Non-invasive surveillance of Plasmodium infection by real-time PCR analysis of ethanol preserved faeces from Ugandan school children with intestinal schistosomiasis

Authors: Hajri Al-Shehri, B. Joanne Power, John Archer, Alice Cousins, Aaron Atuhaire, Moses Adriko, Moses Arinaitwe, Abdullah D. Alanazi, E. James LaCourse, Narcis B. Kabatereine, J. Russell Stothard

Published in: Malaria Journal | Issue 1/2019

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Abstract

Background

As part of ongoing co-surveillance of intestinal schistosomiasis and malaria in Ugandan school children, a non-invasive detection method for amplification of Plasmodium DNA using real-time (rt)PCR analysis of ethanol preserved faeces (EPF) was assessed. For diagnostic tabulations, results were compared to rtPCR analysis of dried blood spots (DBS) and field-based point-of-care (POC) rapid diagnostic tests (RDTs).

Methods

A total of 247 school children from 5 primary schools along the shoreline of Lake Albert were examined with matched EPF and DBS obtained. Mean prevalence and prevalence by school was calculated by detection of Plasmodium DNA by rtPCR using a 18S rDNA Taqman® probe. Diagnostic sensitivity, specificity, positive and negative predictive values were tabulated and compared against RDTs.

Results

By rtPCR of EPF and DBS, 158 (63.9%; 95% CI 57.8–69.7) and 198 (80.1%, 95% CI 74.7–84.6) children were positive for Plasmodium spp. By RDT, 138 (55.8%; 95% CI 49.6–61.9) and 45 (18.2%; 95% CI 13.9–23.5) children were positive for Plasmodium falciparum, and with non-P. falciparum co-infections, respectively. Using RDT results as a convenient field-based reference, the sensitivity of rtPCR of EPF and DBS was 73.1% (95% CI 65.2–79.8) and 94.2% (95% CI 88.9–97.0) while specificity was 47.7% (95% CI 38.5–57.0) and 37.6% (95% CI 29.0–46.9), respectively. With one exception, school prevalence estimated by analysis of EPF was higher than that by RDT. Positive and negative predictive values were compared and discussed.

Conclusions

In this high transmission setting, EPF sampling with rtPCR analysis has satisfactory diagnostic performance in estimation of mean prevalence and prevalence by school upon direct comparison with POC-RDTs. Although analysis of EPF was judged inferior to that of DBS, it permits an alternative non-invasive sampling regime that could be implemented alongside general monitoring and surveillance for other faecal parasites. EPF analysis may also have future value in passive surveillance of low transmission settings.
Literature
2.
go back to reference Christiansen-Jucht C, Parham PE, Saddler A, Koella JC, Basáñez M-G. Temperature during larval development and adult maintenance influences the survival of Anopheles gambiae ss. Parasit Vectors. 2014;7:489.CrossRef Christiansen-Jucht C, Parham PE, Saddler A, Koella JC, Basáñez M-G. Temperature during larval development and adult maintenance influences the survival of Anopheles gambiae ss. Parasit Vectors. 2014;7:489.CrossRef
4.
go back to reference Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS ONE. 2010;5:e8988.CrossRef Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS ONE. 2010;5:e8988.CrossRef
5.
go back to reference Nmadu P, Peter E, Alexander P, Koggie A, Maikenti J. The prevalence of malaria in children between the ages 2-15 visiting Gwarinpa General Hospital life-camp, Abuja, Nigeria. J Health Sci. 2015;5:47–51. Nmadu P, Peter E, Alexander P, Koggie A, Maikenti J. The prevalence of malaria in children between the ages 2-15 visiting Gwarinpa General Hospital life-camp, Abuja, Nigeria. J Health Sci. 2015;5:47–51.
6.
go back to reference Roberts D, Matthews G. Risk factors of malaria in children under the age of five years old in Uganda. Malar J. 2016;15:246.CrossRef Roberts D, Matthews G. Risk factors of malaria in children under the age of five years old in Uganda. Malar J. 2016;15:246.CrossRef
7.
go back to reference Britton S, Cheng Q, McCarthy JS. Novel molecular diagnostic tools for malaria elimination: a review of options from the point of view of high-throughput and applicability in resource limited settings. Malar J. 2016;15:88.CrossRef Britton S, Cheng Q, McCarthy JS. Novel molecular diagnostic tools for malaria elimination: a review of options from the point of view of high-throughput and applicability in resource limited settings. Malar J. 2016;15:88.CrossRef
8.
go back to reference Golassa L, Enweji N, Erko B, Aseffa A, Swedberg G. Detection of a substantial number of sub-microscopic Plasmodium falciparum infections by polymerase chain reaction: a potential threat to malaria control and diagnosis in Ethiopia. Malar J. 2013;12:352.CrossRef Golassa L, Enweji N, Erko B, Aseffa A, Swedberg G. Detection of a substantial number of sub-microscopic Plasmodium falciparum infections by polymerase chain reaction: a potential threat to malaria control and diagnosis in Ethiopia. Malar J. 2013;12:352.CrossRef
9.
go back to reference Bousema T, Okell L, Felger I, Drakeley C. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat Rev Microbiol. 2014;12:833–40.CrossRef Bousema T, Okell L, Felger I, Drakeley C. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat Rev Microbiol. 2014;12:833–40.CrossRef
10.
go back to reference Hofmann NE, Gruenberg M, Nate E, Ura A, Rodriguez-Rodriguez D, Salib M, et al. Assessment of ultra-sensitive malaria diagnosis versus standard molecular diagnostics for malaria elimination: an in-depth molecular community cross-sectional study. Lancet Infect Dis. 2018;18:1108–16.CrossRef Hofmann NE, Gruenberg M, Nate E, Ura A, Rodriguez-Rodriguez D, Salib M, et al. Assessment of ultra-sensitive malaria diagnosis versus standard molecular diagnostics for malaria elimination: an in-depth molecular community cross-sectional study. Lancet Infect Dis. 2018;18:1108–16.CrossRef
11.
go back to reference Buppan P, Putaporntip C, Pattanawong U, Seethamchai S, Jongwutiwes S. Comparative detection of Plasmodium vivax and Plasmodium falciparum DNA in saliva and urine samples from symptomatic malaria patients in a low endemic area. Malar J. 2010;9:72.CrossRef Buppan P, Putaporntip C, Pattanawong U, Seethamchai S, Jongwutiwes S. Comparative detection of Plasmodium vivax and Plasmodium falciparum DNA in saliva and urine samples from symptomatic malaria patients in a low endemic area. Malar J. 2010;9:72.CrossRef
12.
go back to reference Lloyd YM, Esemu LF, Antallan J, Thomas B, Yunga ST, Obase B, et al. PCR-based detection of Plasmodium falciparum in saliva using mitochondrial cox3 and varATS primers. Trop Med Health. 2018;46:22.CrossRef Lloyd YM, Esemu LF, Antallan J, Thomas B, Yunga ST, Obase B, et al. PCR-based detection of Plasmodium falciparum in saliva using mitochondrial cox3 and varATS primers. Trop Med Health. 2018;46:22.CrossRef
13.
go back to reference Talisuna AO, Noor AM, Okui AP, Snow RW. The past, present and future use of epidemiological intelligence to plan malaria vector control and parasite prevention in Uganda. Malar J. 2015;14:158.CrossRef Talisuna AO, Noor AM, Okui AP, Snow RW. The past, present and future use of epidemiological intelligence to plan malaria vector control and parasite prevention in Uganda. Malar J. 2015;14:158.CrossRef
14.
go back to reference Stensgaard AS, Vounatsou P, Onapa AW, Simonsen PE, Pedersen EM, Rahbek C, et al. Bayesian geostatistical modelling of malaria and lymphatic filariasis infections in Uganda: predictors of risk and geographical patterns of co-endemicity. Malar J. 2011;10:298.CrossRef Stensgaard AS, Vounatsou P, Onapa AW, Simonsen PE, Pedersen EM, Rahbek C, et al. Bayesian geostatistical modelling of malaria and lymphatic filariasis infections in Uganda: predictors of risk and geographical patterns of co-endemicity. Malar J. 2011;10:298.CrossRef
15.
go back to reference Al-Shehri H, Stanton MC, LaCourse JE, Atuhaire A, Arinaitwe M, Wamboko A, et al. An extensive burden of giardiasis associated with intestinal schistosomiasis and anaemia in school children on the shoreline of Lake Albert, Uganda. Trans R Soc Trop Med Hyg. 2016;110:597–603.CrossRef Al-Shehri H, Stanton MC, LaCourse JE, Atuhaire A, Arinaitwe M, Wamboko A, et al. An extensive burden of giardiasis associated with intestinal schistosomiasis and anaemia in school children on the shoreline of Lake Albert, Uganda. Trans R Soc Trop Med Hyg. 2016;110:597–603.CrossRef
16.
go back to reference Kabatereine NB, Tukahebwa E, Kazibwe F, Namwangye H, Zaramba S, Brooker S, et al. Progress towards countrywide control of schistosomiasis and soil-transmitted helminthiasis in Uganda. Trans R Soc Trop Med Hyg. 2006;100:208–15.CrossRef Kabatereine NB, Tukahebwa E, Kazibwe F, Namwangye H, Zaramba S, Brooker S, et al. Progress towards countrywide control of schistosomiasis and soil-transmitted helminthiasis in Uganda. Trans R Soc Trop Med Hyg. 2006;100:208–15.CrossRef
17.
go back to reference Koukounari A, Fenwick A, Whawell S, Kabatereine NB, Kazibwe F, Tukahebwa EM, et al. Morbidity indicators of Schistosoma mansoni: relationship between infection and anemia in Ugandan schoolchildren before and after praziquantel and albendazole chemotherapy. Am J Trop Med Hyg. 2006;75:278–86.CrossRef Koukounari A, Fenwick A, Whawell S, Kabatereine NB, Kazibwe F, Tukahebwa EM, et al. Morbidity indicators of Schistosoma mansoni: relationship between infection and anemia in Ugandan schoolchildren before and after praziquantel and albendazole chemotherapy. Am J Trop Med Hyg. 2006;75:278–86.CrossRef
18.
go back to reference Betson M, Clifford S, Stanton M, Kabatereine NB, Stothard JR. Emergence of nonfalciparum Plasmodium infection despite regular artemisinin combination therapy in an 18-month longitudinal study of Ugandan children and their mothers. J Infect Dis. 2018;217:1099–109.CrossRef Betson M, Clifford S, Stanton M, Kabatereine NB, Stothard JR. Emergence of nonfalciparum Plasmodium infection despite regular artemisinin combination therapy in an 18-month longitudinal study of Ugandan children and their mothers. J Infect Dis. 2018;217:1099–109.CrossRef
19.
go back to reference Betson M, Sousa-Figueiredo JC, Atuhaire A, Arinaitwe M, Adriko M, Mwesigwa G, et al. Detection of persistent Plasmodium spp. infections in Ugandan children after artemether-lumefantrine treatment. Parasitology. 2014;141:1880–90.CrossRef Betson M, Sousa-Figueiredo JC, Atuhaire A, Arinaitwe M, Adriko M, Mwesigwa G, et al. Detection of persistent Plasmodium spp. infections in Ugandan children after artemether-lumefantrine treatment. Parasitology. 2014;141:1880–90.CrossRef
20.
go back to reference Sousa-Figueiredo JC, Oguttu D, Adriko M, Besigye F, Nankasi A, Arinaitwe M, et al. Investigating portable fluorescent microscopy (CyScope®) as an alternative rapid diagnostic test for malaria in children and women of child-bearing age. Malar J. 2010;9:245.CrossRef Sousa-Figueiredo JC, Oguttu D, Adriko M, Besigye F, Nankasi A, Arinaitwe M, et al. Investigating portable fluorescent microscopy (CyScope®) as an alternative rapid diagnostic test for malaria in children and women of child-bearing age. Malar J. 2010;9:245.CrossRef
21.
go back to reference Oguike MC, Betson M, Burke M, Nolder D, Stothard JR, Kleinschmidt I, et al. Plasmodium ovale curtisi and Plasmodium ovale wallikeri circulate simultaneously in African communities. Int J Parasitol. 2011;41:677–83.CrossRef Oguike MC, Betson M, Burke M, Nolder D, Stothard JR, Kleinschmidt I, et al. Plasmodium ovale curtisi and Plasmodium ovale wallikeri circulate simultaneously in African communities. Int J Parasitol. 2011;41:677–83.CrossRef
23.
go back to reference Cunningham LJ, Odoom J, Pratt D, Boatemaa L, Asante-Ntim N, Attiku K, et al. Expanding molecular diagnostics of helminthiasis: piloting use of the GPLN platform for surveillance of soil transmitted helminthiasis and schistosomiasis in Ghana. PLos Negl Trop Dis. 2018;12:e0006129.CrossRef Cunningham LJ, Odoom J, Pratt D, Boatemaa L, Asante-Ntim N, Attiku K, et al. Expanding molecular diagnostics of helminthiasis: piloting use of the GPLN platform for surveillance of soil transmitted helminthiasis and schistosomiasis in Ghana. PLos Negl Trop Dis. 2018;12:e0006129.CrossRef
24.
go back to reference Sturrock HJW, Gething PW, Ashton RA, Kolaczinski JH, Kabatereine NB, Brooker S. Planning schistosomiasis control: investigation of alternative sampling strategies for Schistosoma mansoni to target mass drug administration of praziquantel in East Africa. Int Health. 2011;3:165–75.CrossRef Sturrock HJW, Gething PW, Ashton RA, Kolaczinski JH, Kabatereine NB, Brooker S. Planning schistosomiasis control: investigation of alternative sampling strategies for Schistosoma mansoni to target mass drug administration of praziquantel in East Africa. Int Health. 2011;3:165–75.CrossRef
25.
go back to reference Jirků M, Pomajbíková K, Petrželková KJ, Hůzová Z, Modrý D, Lukeš J. Detection of Plasmodium spp. in human feces. Emerg Infect Dis. 2012;18:634.CrossRef Jirků M, Pomajbíková K, Petrželková KJ, Hůzová Z, Modrý D, Lukeš J. Detection of Plasmodium spp. in human feces. Emerg Infect Dis. 2012;18:634.CrossRef
26.
go back to reference Abkallo HM, Liu WM, Hokama S, Ferreira PE, Nakazawa S, Maeno Y, et al. DNA from pre-erythrocytic stage malaria parasites is detectable by PCR in the faeces and blood of hosts. Int J Parasitol. 2014;44:467–73.CrossRef Abkallo HM, Liu WM, Hokama S, Ferreira PE, Nakazawa S, Maeno Y, et al. DNA from pre-erythrocytic stage malaria parasites is detectable by PCR in the faeces and blood of hosts. Int J Parasitol. 2014;44:467–73.CrossRef
27.
go back to reference Keita AK, Fenollar F, Socolovschi C, Ratmanov P, Bassene H, Sokhna C, et al. The detection of vector-borne-disease-related DNA in human stool paves the way to large epidemiological studies. Eur J Epidemiol. 2015;30:1021–6.CrossRef Keita AK, Fenollar F, Socolovschi C, Ratmanov P, Bassene H, Sokhna C, et al. The detection of vector-borne-disease-related DNA in human stool paves the way to large epidemiological studies. Eur J Epidemiol. 2015;30:1021–6.CrossRef
28.
go back to reference Boundenga L, Ollomo B, Rougeron V, Mouele LY, Mve-Ondo B, Delicat-Loembet LM, et al. Diversity of malaria parasites in great apes in Gabon. Malar J. 2015;14:111.CrossRef Boundenga L, Ollomo B, Rougeron V, Mouele LY, Mve-Ondo B, Delicat-Loembet LM, et al. Diversity of malaria parasites in great apes in Gabon. Malar J. 2015;14:111.CrossRef
29.
go back to reference Kaiser M, Löwa A, Ulrich M, Ellerbrok H, Goffe AS, Blasse A, et al. Wild chimpanzees infected with 5 Plasmodium species. Emerg Infect Dis. 2010;16:1956.CrossRef Kaiser M, Löwa A, Ulrich M, Ellerbrok H, Goffe AS, Blasse A, et al. Wild chimpanzees infected with 5 Plasmodium species. Emerg Infect Dis. 2010;16:1956.CrossRef
30.
go back to reference Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature. 2010;467:420.CrossRef Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature. 2010;467:420.CrossRef
31.
go back to reference Loy DE, Liu W, Li Y, Learn GH, Plenderleith LJ, Sundararaman SA, et al. Out of Africa: origins and evolution of the human malaria parasites Plasmodium falciparum and Plasmodium vivax. Int J Parasitol. 2017;47:87–97.CrossRef Loy DE, Liu W, Li Y, Learn GH, Plenderleith LJ, Sundararaman SA, et al. Out of Africa: origins and evolution of the human malaria parasites Plasmodium falciparum and Plasmodium vivax. Int J Parasitol. 2017;47:87–97.CrossRef
32.
go back to reference Kabatereine NB, Brooker S, Koukounari A, Kazibwe F, Tukahebwa EM, Fleming FM, et al. Impact of a national helminth control programme on infection and morbidity in Ugandan schoolchildren. Bull World Health Organ. 2007;85:91–9.CrossRef Kabatereine NB, Brooker S, Koukounari A, Kazibwe F, Tukahebwa EM, Fleming FM, et al. Impact of a national helminth control programme on infection and morbidity in Ugandan schoolchildren. Bull World Health Organ. 2007;85:91–9.CrossRef
33.
go back to reference Verweij JJ, Blangé RA, Templeton K, Schinkel J, Brienen EA, van Rooyen MA, et al. Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol. 2004;42:1220–3.CrossRef Verweij JJ, Blangé RA, Templeton K, Schinkel J, Brienen EA, van Rooyen MA, et al. Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol. 2004;42:1220–3.CrossRef
34.
go back to reference Strøm GE, Tellevik MG, Hanevik K, Langeland N, Blomberg B. Comparison of four methods for extracting DNA from dried blood on filter paper for PCR targeting the mitochondrial Plasmodium genome. Trans R Soc Trop Med Hyg. 2014;108:488–94.CrossRef Strøm GE, Tellevik MG, Hanevik K, Langeland N, Blomberg B. Comparison of four methods for extracting DNA from dried blood on filter paper for PCR targeting the mitochondrial Plasmodium genome. Trans R Soc Trop Med Hyg. 2014;108:488–94.CrossRef
35.
go back to reference Shokoples SE, Ndao M, Kowalewska-Grochowska K, Yanow SK. Multiplexed real-time PCR assay for discrimination of Plasmodium species with improved sensitivity for mixed infections. J Clin Microbiol. 2009;47:975–80.CrossRef Shokoples SE, Ndao M, Kowalewska-Grochowska K, Yanow SK. Multiplexed real-time PCR assay for discrimination of Plasmodium species with improved sensitivity for mixed infections. J Clin Microbiol. 2009;47:975–80.CrossRef
36.
go back to reference Doctor SM, Liu Y, Whitesell A, Thwai KL, Taylor SM, Janko M, et al. Malaria surveillance in the Democratic Republic of the Congo: comparison of microscopy, PCR, and rapid diagnostic test. Diagn Microbiol Infect Dis. 2016;85:16–8.CrossRef Doctor SM, Liu Y, Whitesell A, Thwai KL, Taylor SM, Janko M, et al. Malaria surveillance in the Democratic Republic of the Congo: comparison of microscopy, PCR, and rapid diagnostic test. Diagn Microbiol Infect Dis. 2016;85:16–8.CrossRef
37.
go back to reference Fancony C, Sebastiao YV, Pires JE, Gamboa D, Nery SV. Performance of microscopy and RDTs in the context of a malaria prevalence survey in Angola: a comparison using PCR as the gold standard. Malar J. 2013;12:284.CrossRef Fancony C, Sebastiao YV, Pires JE, Gamboa D, Nery SV. Performance of microscopy and RDTs in the context of a malaria prevalence survey in Angola: a comparison using PCR as the gold standard. Malar J. 2013;12:284.CrossRef
38.
go back to reference Coulibaly JT, Ouattara M, Keiser J, Bonfoh B, N’Goran EK, Andrews JR, et al. Evaluation of malaria diagnoses using a handheld light microscope in a community-based setting in rural Cote d’Ivoire. Am J Trop Med Hyg. 2016;95:831–4.CrossRef Coulibaly JT, Ouattara M, Keiser J, Bonfoh B, N’Goran EK, Andrews JR, et al. Evaluation of malaria diagnoses using a handheld light microscope in a community-based setting in rural Cote d’Ivoire. Am J Trop Med Hyg. 2016;95:831–4.CrossRef
39.
go back to reference Stothard JR, Nabatte B, Sousa-Figueiredo JC, Kabatereine NB. Towards malaria microscopy at the point-of-contact: an assessment of the diagnostic performance of the Newton Nm1 microscope in Uganda. Parasitology. 2014;141:1819–25.CrossRef Stothard JR, Nabatte B, Sousa-Figueiredo JC, Kabatereine NB. Towards malaria microscopy at the point-of-contact: an assessment of the diagnostic performance of the Newton Nm1 microscope in Uganda. Parasitology. 2014;141:1819–25.CrossRef
40.
go back to reference Drakeley CJ, Carneiro I, Reyburn H, Malima R, Lusingu JP, Cox J, et al. Altitude-dependent and-independent variations in Plasmodium falciparum prevalence in northeastern Tanzania. J Infect Dis. 2005;191:1589–98.CrossRef Drakeley CJ, Carneiro I, Reyburn H, Malima R, Lusingu JP, Cox J, et al. Altitude-dependent and-independent variations in Plasmodium falciparum prevalence in northeastern Tanzania. J Infect Dis. 2005;191:1589–98.CrossRef
41.
go back to reference Chandler CI, Drakeley CJ, Reyburn H, Carneiro I. The effect of altitude on parasite density case definitions for malaria in northeastern Tanzania. Trop Med Int Health. 2006;11:1178–84.CrossRef Chandler CI, Drakeley CJ, Reyburn H, Carneiro I. The effect of altitude on parasite density case definitions for malaria in northeastern Tanzania. Trop Med Int Health. 2006;11:1178–84.CrossRef
42.
go back to reference Pothin E, Ferguson NM, Drakeley CJ, Ghani AC. Estimating malaria transmission intensity from Plasmodium falciparum serological data using antibody density models. Malar J. 2016;15:79.CrossRef Pothin E, Ferguson NM, Drakeley CJ, Ghani AC. Estimating malaria transmission intensity from Plasmodium falciparum serological data using antibody density models. Malar J. 2016;15:79.CrossRef
43.
go back to reference Omondi CJ, Onguru D, Kamau L, Nanyingi M, Ongamo G, Estambale B. Perennial transmission of malaria in the low altitude areas of Baringo County, Kenya. Malar J. 2017;16:257.CrossRef Omondi CJ, Onguru D, Kamau L, Nanyingi M, Ongamo G, Estambale B. Perennial transmission of malaria in the low altitude areas of Baringo County, Kenya. Malar J. 2017;16:257.CrossRef
44.
go back to reference Al-Shehri H, Koukounari A, Stanton MC, Adriko M, Arinaitwe M, Atuhaire A, et al. Surveillance of intestinal schistosomiasis during control: a comparison of four diagnostic tests across five Ugandan primary schools in the Lake Albert region. Parasitology. 2018;145:1715–22.CrossRef Al-Shehri H, Koukounari A, Stanton MC, Adriko M, Arinaitwe M, Atuhaire A, et al. Surveillance of intestinal schistosomiasis during control: a comparison of four diagnostic tests across five Ugandan primary schools in the Lake Albert region. Parasitology. 2018;145:1715–22.CrossRef
45.
go back to reference Wilson S, Dunne DW. Advances in our understanding of the epidemiology of Plasmodium and schistosome infection: informing coinfection studies. Curr Opin HIVAIDS. 2012;7:225–30.CrossRef Wilson S, Dunne DW. Advances in our understanding of the epidemiology of Plasmodium and schistosome infection: informing coinfection studies. Curr Opin HIVAIDS. 2012;7:225–30.CrossRef
46.
go back to reference Standley CJ, Mugisha L, Dobson AP, Stothard JR. Zoonotic schistosomiasis in non-human primates: past, present and future activities at the human-wildlife interface in Africa. J Helminthol. 2012;86:131–40.CrossRef Standley CJ, Mugisha L, Dobson AP, Stothard JR. Zoonotic schistosomiasis in non-human primates: past, present and future activities at the human-wildlife interface in Africa. J Helminthol. 2012;86:131–40.CrossRef
47.
go back to reference Standley CJ, Mugisha L, Verweij JJ, Adriko M, Arinaitwe M, Rowell C, et al. Confirmed infection with intestinal schistosomiasis in semi-captive wild-born chimpanzees on Ngamba Island, Uganda. Vector-Borne Zoonotic Dis. 2011;11:169–76.CrossRef Standley CJ, Mugisha L, Verweij JJ, Adriko M, Arinaitwe M, Rowell C, et al. Confirmed infection with intestinal schistosomiasis in semi-captive wild-born chimpanzees on Ngamba Island, Uganda. Vector-Borne Zoonotic Dis. 2011;11:169–76.CrossRef
48.
go back to reference Adriko M, Tinkitina B, Arinaitwe M, Kabatereine NB, Nanyunja M, Tukahebwa EM. Impact of a national deworming campaign on the prevalence of soil-transmitted helminthiasis in Uganda (2004–2016): implications for national control programs. PLos Negl Trop Dis. 2018;12:e0006520.CrossRef Adriko M, Tinkitina B, Arinaitwe M, Kabatereine NB, Nanyunja M, Tukahebwa EM. Impact of a national deworming campaign on the prevalence of soil-transmitted helminthiasis in Uganda (2004–2016): implications for national control programs. PLos Negl Trop Dis. 2018;12:e0006520.CrossRef
49.
go back to reference Ahrberg CD, Ilic BR, Manz A, Neužil P. Handheld real-time PCR device. Lab Chip. 2016;16:586–92.CrossRef Ahrberg CD, Ilic BR, Manz A, Neužil P. Handheld real-time PCR device. Lab Chip. 2016;16:586–92.CrossRef
50.
go back to reference Li T-J, Chang C-M, Chang P-Y, Chuang Y-C, Huang C-C, Su W-C, et al. Handheld energy-efficient magneto-optical real-time quantitative PCR device for target DNA enrichment and quantification. NPG Asia Mater. 2016;8:e277.CrossRef Li T-J, Chang C-M, Chang P-Y, Chuang Y-C, Huang C-C, Su W-C, et al. Handheld energy-efficient magneto-optical real-time quantitative PCR device for target DNA enrichment and quantification. NPG Asia Mater. 2016;8:e277.CrossRef
51.
go back to reference Staedke SG, Maiteki-Sebuguzi C, Rehman AM, Kigozi SP, Gonahasa S, Okiring J, et al. Assessment of community-level effects of intermittent preventive treatment for malaria in schoolchildren in Jinja, Uganda (START-IPT trial): a cluster-randomised trial. Lancet Glob Health. 2018;6:E668–79.CrossRef Staedke SG, Maiteki-Sebuguzi C, Rehman AM, Kigozi SP, Gonahasa S, Okiring J, et al. Assessment of community-level effects of intermittent preventive treatment for malaria in schoolchildren in Jinja, Uganda (START-IPT trial): a cluster-randomised trial. Lancet Glob Health. 2018;6:E668–79.CrossRef
52.
go back to reference Vetter P, Fischer WA, Schibler M, Jacobs M, Bausch DG, Kaiser L. Ebola Virus shedding and transmission: review of current evidence. J Infect Dis. 2016;214:S177–84.CrossRef Vetter P, Fischer WA, Schibler M, Jacobs M, Bausch DG, Kaiser L. Ebola Virus shedding and transmission: review of current evidence. J Infect Dis. 2016;214:S177–84.CrossRef
53.
go back to reference Kabatereine NB, Standley CJ, Sousa-Figueiredo JC, Fleming FM, Stothard JR, Talisuna A, et al. Integrated prevalence mapping of schistosomiasis, soil-transmitted helminthiasis and malaria in lakeside and island communities in Lake Victoria, Uganda. Parasit Vectors. 2011;4:232.CrossRef Kabatereine NB, Standley CJ, Sousa-Figueiredo JC, Fleming FM, Stothard JR, Talisuna A, et al. Integrated prevalence mapping of schistosomiasis, soil-transmitted helminthiasis and malaria in lakeside and island communities in Lake Victoria, Uganda. Parasit Vectors. 2011;4:232.CrossRef
Metadata
Title
Non-invasive surveillance of Plasmodium infection by real-time PCR analysis of ethanol preserved faeces from Ugandan school children with intestinal schistosomiasis
Authors
Hajri Al-Shehri
B. Joanne Power
John Archer
Alice Cousins
Aaron Atuhaire
Moses Adriko
Moses Arinaitwe
Abdullah D. Alanazi
E. James LaCourse
Narcis B. Kabatereine
J. Russell Stothard
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2019
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-019-2748-4

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