Author:
- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- Ethical statement and sample collection.
- Agar plate culture technique and worm collection.
- Formalin-ethyl acetate concentration technique.
- Spiking of human stool with S. stercoralis.
- Sources of DNA and DNA extraction.
- Primer and probe design.
- Real-time PCR.
- Droplet digital PCR assay for S. stercoralis detection.
- Analytical sensitivity and specificity of ddPCR.
- Statistical analysis.
- RESULTS
- DISCUSSION
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Becker SL et al.2015. Real-time PCR for detection of Strongyloides stercoralis in human stool samples from Cote d’Ivoire: diagnostic accuracy, inter-laboratory comparison and patterns of hookworm co-infection. Acta Trop 150: 210–217.
-
2.
Jongsuksuntigul P, Intapan PM, Wongsaroj T, Nilpan S, Singthong S, Veerakul S, Maleewong W, 2003. Prevalence of Strongyloides stercoralis infection in northeastern Thailand (agar plate culture detection). J Med Assoc Thai 86: 737–741.
-
3.
Nontasut P, Muennoo C, Sa-nguankiat S, Fongsri S, Vichit A, 2005. Prevalence of Strongyloides in northern Thailand and treatment with ivermectin vs. albendazole. Southeast Asian J Trop Med Public Health 36: 442–444.
-
4.
Beknazarova M, Whiley H, Ross K, 2016. Strongyloidiasis: a disease of socioeconomic disadvantage. Int J Environ Res Public Health 13: 517.
-
5.
Prasongdee TK, Laoraksawong P, Kanarkard W, Kraiklang R, Sathapornworachai K, Naonongwai S, Laummaunwai P, Sanpool O, Intapan PM, Maleewong W, 2017. An eleven-year retrospective hospital-based study of epidemiological data regarding human strongyloidiasis in northeast Thailand. BMC Infect Dis 17: 627.
-
6.
Hauber HP, Galle J, Chiodini PL, Rupp J, Birke R, Vollmer E, Zabel P, Lange C, 2005. Fatal outcome of a hyperinfection syndrome despite successful eradication of Strongyloides with subcutaneous ivermectin. Infection 33: 383–386.
-
7.
Mejia R, Nutman TB, 2012. Screening, prevention, and treatment for hyperinfection syndrome and disseminated infections caused by Strongyloides stercoralis. Curr Opin Infect Dis 25: 458–463.
-
8.
Mendes T, Minori K, Ueta M, Miguel DC, Allegretti SM, 2017. Strongyloidiasis current status with emphasis in diagnosis and drug research. J Parasitol Res 2017: 5056314.
-
9.
Requena-Mendez A, Chiodini P, Bisoffi Z, Buonfrate D, Gotuzzo E, Munoz J, 2013. The laboratory diagnosis and follow up of strongyloidiasis: a systematic review. PLoS Negl Trop Dis 7: e2002.
-
10.
Chaves LA, Goncalves AL, Paula FM, Silva NM, Silva CV, Costa-Cruz JM, Freitas MA, 2015. Comparison of parasitological, immunological and molecular methods for evaluation of fecal samples of immunosuppressed rats experimentally infected with Strongyloides venezuelensis. Parasitology 142: 1715–1721.
-
11.
Agrawal V, Agarwal T, Ghoshal UC, 2009. Intestinal strongyloidiasis: a diagnosis frequently missed in the tropics. Trans R Soc Trop Med Hyg 103: 242–246.
-
12.
Bisoffi Z et al.2014. Diagnostic accuracy of five serologic tests for Strongyloides stercoralis infection. PLoS Negl Trop Dis 8: e2640.
-
13.
Buonfrate D et al.2015. Accuracy of five serologic tests for the follow up of Strongyloides stercoralis infection. PLoS Negl Trop Dis 9: e0003491.
-
14.
Eamudomkarn C, Sithithaworn P, Sithithaworn J, Kaewkes S, Sripa B, Itoh M, 2015. Comparative evaluation of Strongyloides ratti and S. stercoralis larval antigen for diagnosis of strongyloidiasis in an endemic area of opisthorchiasis. Parasitol Res 114: 2543–2551.
-
15.
Paula FM, Malta Fde M, Marques PD, Sitta RB, Pinho JR, Gryschek RC, Chieffi PP, 2015. Molecular diagnosis of strongyloidiasis in tropical areas: a comparison of conventional and real-time polymerase chain reaction with parasitological methods. Mem Inst Oswaldo Cruz 110: 272–274.
-
16.
Sitta RB, Malta FM, Pinho JR, Chieffi PP, Gryschek RC, Paula FM, 2014. Conventional PCR for molecular diagnosis of human strongyloidiasis. Parasitology 141: 716–721.
-
17.
Nadir E, Grossman T, Ciobotaro P, Attali M, Barkan D, Bardenstein R, Zimhony O, 2016. Real-time PCR for Strongyloides stercoralis-associated meningitis. Diagn Microbiol Infect Dis 84: 197–199.
-
18.
Verweij JJ, Canales M, Polman K, Ziem J, Brienen EA, Polderman AM, van Lieshout L, 2009. Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Trans R Soc Trop Med Hyg 103: 342–346.
-
19.
Kristanti H, Meyanti F, Wijayanti MA, Mahendradhata Y, Polman K, Chappuis F, Utzinger J, Becker SL, Murhandarwati EEH, 2018. Diagnostic comparison of Baermann funnel, Koga agar plate culture and polymerase chain reaction for detection of human Strongyloides stercoralis infection in Maluku, Indonesia. Parasitol Res 117: 3229–3235.
-
20.
Miotke L, Lau BT, Rumma RT, Ji HP, 2014. High sensitivity detection and quantitation of DNA copy number and single nucleotide variants with single color droplet digital PCR. Anal Chem 86: 2618–2624.
-
21.
Wilson M, Glaser KC, Adams-Fish D, Boley M, Mayda M, Molestina RE, 2015. Development of droplet digital PCR for the detection of Babesia microti and Babesia duncani. Exp Parasitol 149: 24–31.
-
22.
Yang R, Paparini A, Monis P, Ryan U, 2014. Comparison of next-generation droplet digital PCR (ddPCR) with quantitative PCR (qPCR) for enumeration of Cryptosporidium oocysts in faecal samples. Int J Parasitol 44: 1105–1113.
-
23.
Ramirez JD, Herrera G, Hernandez C, Cruz-Saavedra L, Munoz M, Florez C, Butcher R, 2018. Evaluation of the analytical and diagnostic performance of a digital droplet polymerase chain reaction (ddPCR) assay to detect Trypanosoma cruzi DNA in blood samples. PLoS Negl Trop Dis 12: e0007063.
-
24.
Mahendran P, Liew JWK, Amir A, Ching XT, Lau YL, 2020. Droplet digital polymerase chain reaction (ddPCR) for the detection of Plasmodium knowlesi and Plasmodium vivax. Malar J 19: 241.
-
25.
Jongthawin J, Intapan PM, Lulitanond V, Sanpool O, Thanchomnang T, Sadaow L, Maleewong W, 2016. Detection and quantification of Wuchereria bancrofti and Brugia malayi DNA in blood samples and mosquitoes using duplex droplet digital polymerase chain reaction. Parasitol Res 115: 2967–2972.
-
26.
Sithithaworn P, Srisawangwong T, Tesana S, Daenseekaew W, Sithithaworn J, Fujimaki Y, Ando K, 2003. Epidemiology of Strongyloides stercoralis in north-east Thailand: application of the agar plate culture technique compared with the enzyme-linked immunosorbent assay. Trans R Soc Trop Med Hyg 97: 398–402.
-
27.
Elkins DB, Haswell-Elkins MR, Mairiang E, Mairiang P, Sithithaworn P, Kaewkes S, Bhudhisawasdi V, Uttaravichien T, 1990. A high frequency of hepatobiliary disease and suspected cholangiocarcinoma associated with heavy Opisthorchis viverrini infection in a small community in north-east Thailand. Trans R Soc Trop Med Hyg 84: 715–719.
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Boonjaraspinyo S, Boonmars T, Kaewsamut B, Ekobol N, Laummaunwai P, Aukkanimart R, Wonkchalee N, Juasook A, Sriraj P, 2013. A cross-sectional study on intestinal parasitic infections in rural communities, northeast Thailand. Korean J Parasitol 51: 727–734.
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Development and Efficacy of Droplet Digital PCR for Detection of Strongyloides stercoralis in Stool
Kantapong Iamrod
Kantapong Iamrod
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Apisit Chaidee
Apisit Chaidee
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Rucksak Rucksaken
Rucksak Rucksaken
Department of Veterinary Technology, Faculty of Veterinary Technology, Kasetsart University, Bangkok, Thailand;
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Kulthida Y. Kopolrat
Kulthida Y. Kopolrat
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Chanika Worasith
Chanika Worasith
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Phattharaphon Wongphutorn
Phattharaphon Wongphutorn
Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
Biomedical Science Program, Graduate School, Khonkaen University, Khon Kaen, Thailand;
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Kitti Intuyod
Kitti Intuyod
Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Somchai Pinlaor
Somchai Pinlaor
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Jiraporn Sithithaworn
Jiraporn Sithithaworn
Faculty of Medicine, Mahasarakham University, Mahasarakham, Thailand
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Paiboon Sithithaworn
Paiboon Sithithaworn
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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Nuttanan Hongsrichan
Nuttanan Hongsrichan
Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand;
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ABSTRACT.
Human strongyloidiasis is one of the neglected tropical diseases caused by infection with soil-transmitted helminth Strongyloides stercoralis. Conventional stool examination, a method commonly used for diagnosis of S. stercoralis, has low sensitivity, especially in the case of light infections. Herein, we developed the droplet digital polymerase chain reaction (ddPCR) assay to detect S. stercoralis larvae in stool and compared its performance with real-time PCR and stool examination techniques (formalin ethyl-acetate concentration technique [FECT] and agar plate culture [APC]). The ddPCR results showed 98% sensitivity and 90% specificity, and real-time PCR showed 82% sensitivity and 76.7% specificity when compared with the microscopic methods. Moreover, ddPCR could detect a single S. stercoralis larva in feces, and cross-reactions with other parasites were not observed. In conclusion, a novel ddPCR method exhibited high sensitivity and specificity for detection of S. stercoralis in stool samples. This technique may help to improve diagnosis, particularly in cases with light infection. In addition, ddPCR technique might be useful for screening patients before starting immunosuppressive drug therapy, and follow-up after treatment of strongyloidiasis.
Author Notes
Financial support: This work was financially supported by the young researcher development project of Khon Kaen University (2019) and Invitation Research fund (Grant number IN63250) Faculty of Medicine, Khon Kaen University, Thailand.
Authors’ addresses: Kantapong Iamrod, Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand, E-mail: kantapongia@kkumail.com. Apisit Chaidee, Kulthida Y. Kopolrat, Chanika Worasith, Somchai Pinlaor, Paiboon Sithithaworn, and Nuttanan Hongsrichan, Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand, and Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand, E-mails: apisch@kku.ac.th, kulthida_kop@yahoo.com, chanika.w@kkumail.com, psomec@kku.ac.th, paibsit@gmail.com, and nuttho@kku.ac.th. Rucksak Rucksaken, Department of Veterinary Technology, Faculty of Veterinary Technology, Kasetsart University, Bangkok, Thailand, E-mail: lucidlucky@gmail.com. Phattharaphon Wongphutorn, Cholangiocarcinoma Research Institute, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand, and Biomedical Science Program, Graduate School, Khon kaen University, Khon Kaen, Thailand, E-mail: phat_phutorn@hotmail.com. Kitti Intuyod, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand, E-mail: kittin@kku.ac.th. Jiraporn Sithithaworn, Faculty of Medicine, Mahasarakham University, Mahasarakham, Thailand, E-mail: jirapornsith@gmail.com.
- ABSTRACT.
- INTRODUCTION
- MATERIALS AND METHODS
- Ethical statement and sample collection.
- Agar plate culture technique and worm collection.
- Formalin-ethyl acetate concentration technique.
- Spiking of human stool with S. stercoralis.
- Sources of DNA and DNA extraction.
- Primer and probe design.
- Real-time PCR.
- Droplet digital PCR assay for S. stercoralis detection.
- Analytical sensitivity and specificity of ddPCR.
- Statistical analysis.
- RESULTS
- DISCUSSION
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Becker SL et al.2015. Real-time PCR for detection of Strongyloides stercoralis in human stool samples from Cote d’Ivoire: diagnostic accuracy, inter-laboratory comparison and patterns of hookworm co-infection. Acta Trop 150: 210–217.
-
2.
Jongsuksuntigul P, Intapan PM, Wongsaroj T, Nilpan S, Singthong S, Veerakul S, Maleewong W, 2003. Prevalence of Strongyloides stercoralis infection in northeastern Thailand (agar plate culture detection). J Med Assoc Thai 86: 737–741.
-
3.
Nontasut P, Muennoo C, Sa-nguankiat S, Fongsri S, Vichit A, 2005. Prevalence of Strongyloides in northern Thailand and treatment with ivermectin vs. albendazole. Southeast Asian J Trop Med Public Health 36: 442–444.
-
4.
Beknazarova M, Whiley H, Ross K, 2016. Strongyloidiasis: a disease of socioeconomic disadvantage. Int J Environ Res Public Health 13: 517.
-
5.
Prasongdee TK, Laoraksawong P, Kanarkard W, Kraiklang R, Sathapornworachai K, Naonongwai S, Laummaunwai P, Sanpool O, Intapan PM, Maleewong W, 2017. An eleven-year retrospective hospital-based study of epidemiological data regarding human strongyloidiasis in northeast Thailand. BMC Infect Dis 17: 627.
-
6.
Hauber HP, Galle J, Chiodini PL, Rupp J, Birke R, Vollmer E, Zabel P, Lange C, 2005. Fatal outcome of a hyperinfection syndrome despite successful eradication of Strongyloides with subcutaneous ivermectin. Infection 33: 383–386.
-
7.
Mejia R, Nutman TB, 2012. Screening, prevention, and treatment for hyperinfection syndrome and disseminated infections caused by Strongyloides stercoralis. Curr Opin Infect Dis 25: 458–463.
-
8.
Mendes T, Minori K, Ueta M, Miguel DC, Allegretti SM, 2017. Strongyloidiasis current status with emphasis in diagnosis and drug research. J Parasitol Res 2017: 5056314.
-
9.
Requena-Mendez A, Chiodini P, Bisoffi Z, Buonfrate D, Gotuzzo E, Munoz J, 2013. The laboratory diagnosis and follow up of strongyloidiasis: a systematic review. PLoS Negl Trop Dis 7: e2002.
-
10.
Chaves LA, Goncalves AL, Paula FM, Silva NM, Silva CV, Costa-Cruz JM, Freitas MA, 2015. Comparison of parasitological, immunological and molecular methods for evaluation of fecal samples of immunosuppressed rats experimentally infected with Strongyloides venezuelensis. Parasitology 142: 1715–1721.
-
11.
Agrawal V, Agarwal T, Ghoshal UC, 2009. Intestinal strongyloidiasis: a diagnosis frequently missed in the tropics. Trans R Soc Trop Med Hyg 103: 242–246.
-
12.
Bisoffi Z et al.2014. Diagnostic accuracy of five serologic tests for Strongyloides stercoralis infection. PLoS Negl Trop Dis 8: e2640.
-
13.
Buonfrate D et al.2015. Accuracy of five serologic tests for the follow up of Strongyloides stercoralis infection. PLoS Negl Trop Dis 9: e0003491.
-
14.
Eamudomkarn C, Sithithaworn P, Sithithaworn J, Kaewkes S, Sripa B, Itoh M, 2015. Comparative evaluation of Strongyloides ratti and S. stercoralis larval antigen for diagnosis of strongyloidiasis in an endemic area of opisthorchiasis. Parasitol Res 114: 2543–2551.
-
15.
Paula FM, Malta Fde M, Marques PD, Sitta RB, Pinho JR, Gryschek RC, Chieffi PP, 2015. Molecular diagnosis of strongyloidiasis in tropical areas: a comparison of conventional and real-time polymerase chain reaction with parasitological methods. Mem Inst Oswaldo Cruz 110: 272–274.
-
16.
Sitta RB, Malta FM, Pinho JR, Chieffi PP, Gryschek RC, Paula FM, 2014. Conventional PCR for molecular diagnosis of human strongyloidiasis. Parasitology 141: 716–721.
-
17.
Nadir E, Grossman T, Ciobotaro P, Attali M, Barkan D, Bardenstein R, Zimhony O, 2016. Real-time PCR for Strongyloides stercoralis-associated meningitis. Diagn Microbiol Infect Dis 84: 197–199.
-
18.
Verweij JJ, Canales M, Polman K, Ziem J, Brienen EA, Polderman AM, van Lieshout L, 2009. Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Trans R Soc Trop Med Hyg 103: 342–346.
-
19.
Kristanti H, Meyanti F, Wijayanti MA, Mahendradhata Y, Polman K, Chappuis F, Utzinger J, Becker SL, Murhandarwati EEH, 2018. Diagnostic comparison of Baermann funnel, Koga agar plate culture and polymerase chain reaction for detection of human Strongyloides stercoralis infection in Maluku, Indonesia. Parasitol Res 117: 3229–3235.
-
20.
Miotke L, Lau BT, Rumma RT, Ji HP, 2014. High sensitivity detection and quantitation of DNA copy number and single nucleotide variants with single color droplet digital PCR. Anal Chem 86: 2618–2624.
-
21.
Wilson M, Glaser KC, Adams-Fish D, Boley M, Mayda M, Molestina RE, 2015. Development of droplet digital PCR for the detection of Babesia microti and Babesia duncani. Exp Parasitol 149: 24–31.
-
22.
Yang R, Paparini A, Monis P, Ryan U, 2014. Comparison of next-generation droplet digital PCR (ddPCR) with quantitative PCR (qPCR) for enumeration of Cryptosporidium oocysts in faecal samples. Int J Parasitol 44: 1105–1113.
-
23.
Ramirez JD, Herrera G, Hernandez C, Cruz-Saavedra L, Munoz M, Florez C, Butcher R, 2018. Evaluation of the analytical and diagnostic performance of a digital droplet polymerase chain reaction (ddPCR) assay to detect Trypanosoma cruzi DNA in blood samples. PLoS Negl Trop Dis 12: e0007063.
-
24.
Mahendran P, Liew JWK, Amir A, Ching XT, Lau YL, 2020. Droplet digital polymerase chain reaction (ddPCR) for the detection of Plasmodium knowlesi and Plasmodium vivax. Malar J 19: 241.
-
25.
Jongthawin J, Intapan PM, Lulitanond V, Sanpool O, Thanchomnang T, Sadaow L, Maleewong W, 2016. Detection and quantification of Wuchereria bancrofti and Brugia malayi DNA in blood samples and mosquitoes using duplex droplet digital polymerase chain reaction. Parasitol Res 115: 2967–2972.
-
26.
Sithithaworn P, Srisawangwong T, Tesana S, Daenseekaew W, Sithithaworn J, Fujimaki Y, Ando K, 2003. Epidemiology of Strongyloides stercoralis in north-east Thailand: application of the agar plate culture technique compared with the enzyme-linked immunosorbent assay. Trans R Soc Trop Med Hyg 97: 398–402.
-
27.
Elkins DB, Haswell-Elkins MR, Mairiang E, Mairiang P, Sithithaworn P, Kaewkes S, Bhudhisawasdi V, Uttaravichien T, 1990. A high frequency of hepatobiliary disease and suspected cholangiocarcinoma associated with heavy Opisthorchis viverrini infection in a small community in north-east Thailand. Trans R Soc Trop Med Hyg 84: 715–719.
-
28.
Anamnart W, Intapan PM, Maleewong W, 2013. Modified formalin-ether concentration technique for diagnosis of human strongyloidiasis. Korean J Parasitol 51: 743–745.
-
29.
Boonjaraspinyo S, Boonmars T, Kaewsamut B, Ekobol N, Laummaunwai P, Aukkanimart R, Wonkchalee N, Juasook A, Sriraj P, 2013. A cross-sectional study on intestinal parasitic infections in rural communities, northeast Thailand. Korean J Parasitol 51: 727–734.
-
30.
Eamudomkarn C, et al.2018. Diagnostic performance of urinary IgG antibody detection: a novel approach for population screening of strongyloidiasis. PLOS ONE 13: e0192598.
-
31.
McHugh ML, 2012. Interrater reliability: the kappa statistic. Biochem Med (Zagreb) 22: 276–282.
-
32.
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