Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-15T07:24:14.254Z Has data issue: false hasContentIssue false

Intestinal parasites in rural communities in Nan Province, Thailand: changes in bacterial gut microbiota associated with minute intestinal fluke infection

Published online by Cambridge University Press:  04 May 2020

Ajala Prommi
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
Pinidphon Prombutara
Affiliation:
Faculty of Science, Omics Science & Bioinformatics Center, Chulalongkorn University, Bangkok, Thailand Faculty of Science, Microbiome Research Unit for Probiotics in Food and Cosmetics, Chulalongkorn University, Bangkok, Thailand
Dorn Watthanakulpanich
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
Poom Adisakwattana
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
Teera Kusolsuk
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
Tippayarat Yoonuan
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
Akkarin Poodeepiyasawat
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
Nirundorn Homsuwan
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
Samreong Prummongkol
Affiliation:
Faculty of Tropical Medicine, Mahidol Bangkok School of Tropical Medicine, Mahidol University, Bangkok, Thailand
Malee Tanita
Affiliation:
Saen Thong Health Promoting Hospital, Tha Wang Pha, Nan, Thailand
Sungkhom Rattanapikul
Affiliation:
Saen Thong Health Promoting Hospital, Tha Wang Pha, Nan, Thailand
Chuanphot Thinphovong
Affiliation:
Faculty of Veterinary Technology, Kasetsart University, Bangkok, Thailand
Anamika Kritiyakan
Affiliation:
Faculty of Veterinary Technology, Kasetsart University, Bangkok, Thailand
Serge Morand
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand Faculty of Veterinary Technology, Kasetsart University, Bangkok, Thailand Faculty of Veterinary Technology, CNRS ISEM – CIRAD ASTRE, Kasetsart University, Bangkok, Thailand
Kittipong Chaisiri*
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
*
Author for correspondence: Kittipong Chaisiri, E-mail: [email protected]

Abstract

Gastrointestinal helminth infection likely affects the gut microbiome, in turn affecting host health. To investigate the effect of intestinal parasite status on the gut microbiome, parasitic infection surveys were conducted in communities in Nan Province, Thailand. In total, 1047 participants submitted stool samples for intestinal parasite examination, and 391 parasite-positive cases were identified, equating to an infection prevalence of 37.3%. Intestinal protozoan species were less prevalent (4.6%) than helminth species. The most prevalent parasite was the minute intestinal fluke Haplorchis taichui (35.9%). Amplicon sequencing of 16S rRNA was conducted to investigate the gut microbiome profiles of H. taichui-infected participants compared with those of parasite-free participants. Prevotella copri was the dominant bacterial operational taxonomic unit (OTU) in the study population. The relative abundance of three bacterial taxa, Ruminococcus, Roseburia faecis and Veillonella parvula, was significantly increased in the H. taichui-infected group. Parasite-negative group had higher bacterial diversity (α diversity) than the H. taichui-positive group. In addition, a significant difference in bacterial community composition (β diversity) was found between the two groups. The results suggest that H. taichui infection impacts the gut microbiome profile by reducing bacterial diversity and altering bacterial community structure in the gastrointestinal tract.

Type
Research Article
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aivelo, T and Norberg, A (2016) Parasite–microbiota interactions potentially affect intestinal communities in wild mammals. Journal of Animal Ecology 87, 438447.CrossRefGoogle Scholar
Alpizar-Rodriguez, D, Lesker, TR, Gronow, A, Gilbert, B, Raemy, E, Lamacchia, C, Gabay, C, Finckh, A and Strowig, T (2019) Prevotella copri in individuals at risk for rheumatoid arthritis. Annals of the Rheumatic Diseases 78, 590593.CrossRefGoogle ScholarPubMed
Bolyen, E, Rideout, JR, Dillon, MR, Bokulich, NA, Abnet, CC, Al-Ghalith, GA, Alexander, H, Alm, EJ, Arumugam, M, Asnicar, F, Bai, Y, Bisanz, JE, Bittinger, K, Brejnrod, A, Brislawn, CJ, Brown, CT, Callahan, BJ, Caraballo-Rodríguez, AM, Chase, J, Cope, EK, Da Silva, R, Diener, C, Dorrestein, PC, Douglas, GM, Durall, DM, Duvallet, C, Edwardson, CF, Ernst, M, Estaki, M, Fouquier, J, Gauglitz, JM, Gibbons, SM, Gibson, DL, Gonzalez, A, Gorlick, K, Guo, J, Hillmann, B, Holmes, S, Holste, H, Huttenhower, C, Huttley, GA, Janssen, S, Jarmusch, AK, Jiang, L, Kaehler, BD, Kang, KB, Keefe, CR, Keim, P, Kelley, ST, Knights, D, Koester, I, Kosciolek, T, Kreps, J, Langille, MGI, Lee, J, Ley, R, Liu, YX, Loftfield, E, Lozupone, C, Maher, M, Marotz, C, Martin, BD, McDonald, D, McIver, LJ, Melnik, AV, Metcalf, JL, Morgan, SC, Morton, JT, Naimey, AT, Navas-Molina, JA, Nothias, LF, Orchanian, SB, Pearson, T, Peoples, SL, Petras, D, Preuss, ML, Pruesse, E, Rasmussen, LB, Rivers, A, Robeson, MS, Rosenthal, P, Segata, N, Shaffer, M, Shiffer, A, Sinha, R, Song, SJ, Spear, JR, Swafford, AD, Thompson, LR, Torres, PJ, Trinh, P, Tripathi, A, Turnbaugh, PJ, Ul-Hasan, S, van der Hooft, JJJ, Vargas, F, Vázquez-Baeza, Y, Vogtmann, E, von Hippel, M, Walters, W, Wan, Y, Wang, M, Warren, J, Weber, KC, Williamson, CHD, Willis, AD, Xu, ZZ, Zaneveld, JR, Zhang, Y, Zhu, Q, Knight, R and Caporaso, JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology 37, 852857.CrossRefGoogle ScholarPubMed
Boonmekam, D, Namchote, S, Nak-ai, W, Glaubrecht, M and Krailas, D (2016) The prevalence of human intestinal fluke infections, Haplorchis Taichui, in Thiarid snails and cyprinid fish in Bo Kluea District and Pua District, Nan Province, Thailand. Silpakorn University Science and Technology Journal 10, 2937.Google Scholar
Broadhurst, MJ, Ardeshir, A, Kanwar, B, Mirpuri, J, Gundra, UM, Leung, JM, Wiens, KE, Vujkovic-Cvijin, I, Kim, CC, Yarovinsky, F, Lerche, NW, McCune, JM and Loke, P (2012) Therapeutic helminth infection of macaques with idiopathic chronic diarrhea alters the inflammatory signature and mucosal microbiota of the colon. PLoS Pathogens 8, e1003000.CrossRefGoogle ScholarPubMed
Callahan, BJ, McMurdie, PJ, Rosen, MJ, Han, AW, Johnson, AJ and Holmes, SP (2016) Dada2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581.CrossRefGoogle ScholarPubMed
Cantacessi, C, Giacomin, P, Croese, J, Zakrzewski, M, Sotillo, J, McCann, L, Nolan, MJ, Mitreva, M, Krause, L and Loukas, A (2014) Impact of experimental hookworm infection on the human gut microbiota. Journal of Infectious Diseases 210, 14311434.CrossRefGoogle ScholarPubMed
Caporaso, JG, Lauber, CL, Walters, WA, Berg-Lyons, D, Lozupone, CA, Turnbaugh, PJ, Fierer, N and Knight, R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the USA 108(Suppl), 45164522.CrossRefGoogle Scholar
Cattadori, IM, Sebastian, A, Hao, H, Katani, R, Albert, I, Eilertson, KE, Kapur, V, Pathak, A and Mitchel, S (2016) Impact of helminth infections and nutritional constraints on the small intestine microbiota. PLoS ONE 11, e0159770.CrossRefGoogle ScholarPubMed
Chai, JY, Yong, TS, Eom, KS, Min, DY, Shin, EH, Banouvong, V, Insisiengmay, B, Insisiengmay, S, Phommasack, B and Rim, HJ (2010) Prevalence of the intestinal flukes Haplorchis taichui and H. yokogawai in a mountainous area of Phongsaly Province, Lao PDR. Korean Journal of Parasitology 48, 339342.CrossRefGoogle Scholar
Chaisiri, K, Jollivet, C, Della Rossa, P, Sanguankiat, S, Wattanakulpanich, D, Lajaunie, C, Binot, A, Tanita, M, Rattanapikul, S, Sutdan, D, Morand, S and Ribas, A (2018) Parasitic infections in relation to practices and knowledge in a rural village in Northern Thailand with emphasis on fish-borne trematode infection. Epidemiology and Infection 15, 112.Google Scholar
Chaiyos, J, Suwannatrai, K, Thinkhamrop, K, Pratumchart, K, Sereewong, C, Tesana, S, Kaewkes, S, Sripa, B, Wongsaroj, T and Suwannatrai, AT (2018) Maxent modeling of soil-transmitted helminth infection distributions in Thailand. Parasitology Research 117, 35073517.CrossRefGoogle ScholarPubMed
Cooper, P, Walker, AW, Reyes, J, Chico, M, Salter, SJ, Vaca, M and Parkhill, J (2013) Patent human infections with the whipworm, Trichuris trichiura, are not associated with alterations in the faecal microbiota. PLoS ONE 8, e76573.CrossRefGoogle Scholar
Fu, PP, Xiong, F, Feng, WW, Zou, H, Wu, SG, Li, M, Wang, GT and Li, WX (2019) Effect of intestinal tapeworms on the gut microbiota of the common carp, Cyprinus carpio. Parasites & Vectors 12, 252.CrossRefGoogle ScholarPubMed
Giacomin, P, Zakrzewski, M, Jenkins, TP, Su, X, Al-Hallaf, R, Croese, J, de Vries, S, Grant, A, Mitreva, M, Loukas, A, Krause, L and Cantacessi, C (2016) Changes in duodenal tissue-associated microbiota following hookworm infection and consecutive gluten challenges in humans with coeliac disease. Scientific Reports 6, 36797.CrossRefGoogle ScholarPubMed
Gilbert, JA, Blaser, MJ, Caporaso, JG, Jansson, JK, Lynch, SV and Knight, R (2018) Current understanding of the human microbiome. Nature Medicine 24, 392400.CrossRefGoogle ScholarPubMed
Glendinning, L, Nausch, N, Free, A, Taylor, DW and Mutapi, F (2014) The microbiota and helminths: sharing the same niche in the human host. Parasitology 141, 12551271.CrossRefGoogle ScholarPubMed
Hotez, PJ, Molyneux, DH, Fenwick, A, Ottesen, E, Sachs, SE and Sachs, JD (2006) Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDS, tuberculosis, and malaria: a comprehensive pro-poor health policy and strategy for the developing world. PLoS Medicine 3, e102.CrossRefGoogle Scholar
Hotez, PJ, Brindley, PJ, Bethony, JM, King, CH, Pearce, EJ and Jacobson, J (2008) Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 13111321.CrossRefGoogle ScholarPubMed
Howell, AK, Tongue, SC, Currie, C, Evans, J, Williams, DJL and McNeilly, TN (2018) Co-infection with Fasciola hepatica may increase the risk of Escherichia coli O157 shedding in British cattle destined for the food chain. Preventive Veterinary Medicine 150, 7076.CrossRefGoogle ScholarPubMed
Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486, 207214.CrossRefGoogle Scholar
Illumina (2013) 16S Metagenomic sequencing library preparation guide. Available at https://support.illumina.com/downloads/16s_metagenomic_sequencing_library_preparation.html (Assessed September 2018).Google Scholar
Itthitaetrakool, U, Pinlaor, P, Pinlaor, S, Chomvarin, C, Dangtakot, R, Chaidee, A, Wilailuckana, C, Sangka, A, Lulitanond, A and Yongvanit, P (2016) Chronic Opisthorchis viverrini infection changes the liver microbiome and promotes Helicobacter Growth. PLoS ONE 11, e0165798.CrossRefGoogle ScholarPubMed
Jandhyala, SM, Talukdar, R, Subramanyam, C, Vuyyuru, H, Sasikala, M and Reddy, DN (2015) Role of the normal gut microbiota. World Journal of Gastroenterology 21, 87878803.CrossRefGoogle ScholarPubMed
Jenkins, TP (2019) Exploring the impact of gastrointestinal parasitic helminths on the human microbiome using advanced biomolecular and bioinformatics technologies (PhD thesis). University of Cambridge, Cambridge.Google Scholar
Jenkins, TP, Formenti, F, Castro, C, Piubelli, C, Perandin, F, Buonfrate, D, Otranto, D, Griffin, JL, Krause, L, Bisoffi, Z and Cantacessi, C (2018) A comprehensive analysis of the faecal microbiome and metabolome of Strongyloides stercoralis infected volunteers from a non-endemic area. Scientific Reports 8, 15651.CrossRefGoogle ScholarPubMed
Katz, N, Chaves, A and Pellegrino, J (1972) A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Revista do Instituto de Medicina Tropical de São Paulo 14, 397400.Google ScholarPubMed
Kay, GL, Millard, A, Sergeant, MJ, Midzi, N, Gwisai, R, Mduluza, T, Ivens, A, Nausch, N, Mutapi, F and Pallen, M (2015) Differences in the faecal microbiome in Schistosoma haematobium infected children vs uninfected children. PLoS Neglected Tropical Diseases 9, e0003861.CrossRefGoogle ScholarPubMed
Keiser, PB and Nutman, TB (2004) Strongyloides stercoralis in the immunocompromised population. Clinical Microbiology Reviews 17, 208217.CrossRefGoogle ScholarPubMed
Kreisinger, J, Bastien, G, Hauffe, HC, Marchesi, J and Perkins, SE (2015) Interactions between multiple helminths and the gut microbiota in wild rodents. Philosophical Transactions of the Royal Society B 370, 20140295.CrossRefGoogle ScholarPubMed
Kriss, M, Hazleton, KZ, Nusbacher, NM, Martin, CG and Lozupone, CA (2018) Low diversity gut microbiota dysbiosis: drivers, functional implications and recovery. Current Opinion in Microbiology 44, 3440.CrossRefGoogle ScholarPubMed
Lee, SC, Tang, MS, Lim, YA, Choy, SH, Kurtz, ZD, Cox, LM, Gundra, UM, Cho, I, Bonneau, R, Blaser, MJ, Chua, KH and Loke, P (2014) Helminth colonization is associated with increased diversity of the gut microbiota. PLoS Neglected Tropical Diseases 8, e2880.CrossRefGoogle ScholarPubMed
Li, RW, Li, W, Sun, J, Yu, P, Baldwin, RL and Urban, JF (2016) The effect of helminth infection on the microbial composition and structure of the caprine abomasal microbiome. Scientific Reports 6, 20606.CrossRefGoogle ScholarPubMed
Martin, M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal 17, 1012.CrossRefGoogle Scholar
Martin, I, Kaisar, MMM, Wiria, AE, Hamid, F, Djuardi, Y, Sartono, E, Rosa, BA, Mitreva, M, Supali, T, Houwing-Duistermaat, JJ, Yazdanbakhsh, M and Wammes, LJ (2019) The effect of gut microbiome composition on human immune responses: an exploration of interference by helminth infections. Frontiers in Genetics 10, 1028.CrossRefGoogle ScholarPubMed
Muehlenbachs, A, Bhatnagar, J, Agudelo, CA, Hidron, A, Eberhard, ML, Mathison, BA, Frace, MA, Ito, A, Metcalfe, MG, Rollin, DC, Visvesvara, GS, Pham, CD, Jones, TL, Greer, PW, Vélez Hoyos, A, Olson, PD, Diazgranados, LR and Zaki, SR (2015) Malignant transformation of Hymenolepis nana in a human host. New England Journal of Medicine 373, 18451852.CrossRefGoogle Scholar
Mutapi, F (2015) The gut microbiome in the helminth infected host. Trends in Parasitology 31, 405406.CrossRefGoogle ScholarPubMed
Newbold, LK, Burthe, SJ, Oliver, AE, Gweon, HS, Barnes, CJ, Daunt, F and Van der Gast, CJ (2017) Helminth burden and ecological factors associated with alterations in wild host gastrointestinal microbiota. ISME Journal 11, 663675.CrossRefGoogle ScholarPubMed
Nithikathkul, C, Trevanich, A, Wongsaroj, T, Wongsawad, C and Reungsang, P (2017) Health informatics model for helminthiasis in Thailand. Journal of Helminthology 91, 528533.CrossRefGoogle ScholarPubMed
Pabalan, N, Singian, E, Tabangay, L, Jarjanazi, H, Boivin, MJ and Ezeamama, AE (2017) Soil-transmitted helminth infection, loss of education and cognitive impairment in school-aged children: a systematic review and meta-analysis. PLoS Neglected Tropical Diseases 12, e0005523. https://doi.org/10.1371/journal.pntd.0005523.CrossRefGoogle Scholar
Pal, M, Ayele, Y, Hadush, A, Kundu, P and Jadhav, VJ (2018) Public health significance of foodborne helminthiasis: a systematic review. Journal of Experimental Food Chemistry 4, 135140.CrossRefGoogle Scholar
Punsawad, C, Phasuk, N, Bunratsami, S, Thongtup, K, Viriyavejakul, P, Palipoch, S, Koomhin, P and Nongnaul, S (2018) Prevalence of intestinal parasitic infections and associated risk factors for hookworm infections among primary schoolchildren in rural areas of Nakhon Si Thammarat, southern Thailand. BMC Public Health 18, 1118.CrossRefGoogle ScholarPubMed
Quast, C, Pruesse, E, Yilmaz, P, Gerken, J, Schweer, T, Yarza, P, Peplies, J and Glöckner, FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, 590596.CrossRefGoogle ScholarPubMed
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at http://www.r-project.org/index.html.Google Scholar
Round, JL and Mazmanian, SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nature Reviews Immunology 9, 313323.CrossRefGoogle ScholarPubMed
Rozsa, L, Reiczigel, J and Majoros, G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228232.CrossRefGoogle ScholarPubMed
Sato, M, Sanguankiat, S, Pubampen, S, Kusolsuk, T, Maipanich, W and Waikagul, J (2009) Egg laying capacity of Haplorchis taichui (Digenea: Heterophyidae) in humans. Korean Journal of Parasitology 47, 315318.CrossRefGoogle ScholarPubMed
Schule, SA, Clowes, P, Kroidl, I, Kowuor, DO, Nsojo, A, Mangu, C, Riess, H, Geldmacher, C, Laubender, RP, Mhina, S, Maboko, L, Löscher, T, Hoelscher, M and Saathoff, E (2014) Ascaris lumbricoides infection and its relation to environmental factors in the Mbeya region of Tanzania, a cross-sectional, population-based study. PLoS ONE 9, e92032.CrossRefGoogle ScholarPubMed
Segata, N, Izard, J, Waldron, L, Gevers, D, Miropolsky, L, Garrett, WS and Huttenhower, C (2011) Metagenomic biomarker discovery and explanation. Genome Biology 12, 60.CrossRefGoogle ScholarPubMed
Sripa, B, Kaewkes, S, Sithithaworn, P, Mairiang, E, Laha, T, Smout, M, Pairojkul, C, Bhudhisawasdi, V, Tesana, S, Thinkamrop, B, Bethony, JM, Loukas, A and Brindley, PJ (2007) Liver fluke induces cholangiocarcinoma. PLoS Medicine 4, e201. https://doi.org/10.1371/journal.pmed.0040201.CrossRefGoogle ScholarPubMed
Su, C, Su, L, Li, Y, Long, SR, Chang, J, Zhang, W, Walker, WA, Xavier, RJ, Cherayil, BJ and Shi, HN (2018) Helminth-induced alterations of the gut microbiota exacerbate bacterial colitis. Mucosal Immunology 11, 144157.CrossRefGoogle ScholarPubMed
Tantrawatpan, C, Intapan, PM, Thanchomnang, T, Sanpool, O, Janwan, P, Lulitanond, V, Sadaow, L and Maleewong, W (2014) Development of a PCR assay and pyrosequencing for identification of important human fish-borne trematodes and its potential use for detection in faecal specimens. Parasites & Vectors 7, 8897.CrossRefGoogle Scholar
Truong, DT, Tett, A, Pasolli, E, Huttenhower, C and Segata, N (2017) Microbial strain-level population structure and genetic diversity from metagenomes. Genome Research 27, 626638.CrossRefGoogle ScholarPubMed
Vicente, CS, Ozawa, S and Hasegawa, K (2016) Composition of the cockroach gut microbiome in the presence of parasitic nematodes. Microbes and Environments 31, 314320.CrossRefGoogle ScholarPubMed
Waikagul, J, Jongsuksantigul, P, Rattanawitoon, U, Radomyos, P, Kojima, S and Takeuchi, T (2008) Parasitological monitoring of helminth control program in Northern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 39, 10081014Google ScholarPubMed
Walshe, N, Duggan, V, Cabrera-Rubio, R, Crispie, F, Cotter, P, Feehan, O and Mulcahy, G (2019) Removal of adult cyathostomins alters faecal microbiota and promotes an inflammatory phenotype in horses. International Journal for Parasitology 49, 489500.CrossRefGoogle ScholarPubMed
Wang, S, El-Fahmawi, A, Christian, DA, Fang, Q, Radaelli, E, Chen, L, Sullivan, MC, Misic, AM, Ellringer, JA, Zhu, XQ, Winter, SE, Hunter, CA and Beiting, DP (2019) Infection-induced intestinal dysbiosis is mediated by macrophage activation and nitrate production. mBio 10, e00935–19.CrossRefGoogle ScholarPubMed
Watthanakulpanich, D, Waikagul, J, Maipanich, W, Nuamtanong, S, Sanguankiat, S, Pubampen, S, Praevanit, R, Mongkhonmu, S and Nawa, Y (2010) Haplorchis taichui as a possible etiologic agent of irritable bowel syndrome-like symptoms. Korean Journal of Parasitology 48, 225229.CrossRefGoogle ScholarPubMed
Weldon, L, Abolins, S, Lenzi, L, Bourne, C, Riley, EM and Viney, M (2015) The gut microbiota of wild mice. PLoS ONE 10, e0134643.CrossRefGoogle ScholarPubMed
Wijit, A, Morakote, N and Klinchid, J (2013) High prevalence of haplorchiasis in Nan and Lampang provinces, Thailand, proven by adult worm recovery from suspected opisthorchiasis cases. Korean Journal of Parasitology 51, 767769.CrossRefGoogle ScholarPubMed
Wongsaroj, T, Nithikathkul, C, Rojkitikun, W, Nakaia, W, Royal, L and Rammasut, P (2014) National survey of helminthiasis in Thailand. Asian Biomedicine 8, 779783.CrossRefGoogle Scholar
Wu, HJ and Wu, E (2012) The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes 3, 414.CrossRefGoogle ScholarPubMed
Wu, S, Li, RW, Li, E, Beshah, E, Dawson, HD and Urban, JF (2012) Worm burden-dependent disruption of the porcine colon microbiota by Trichuris suis infection. PLoS ONE 7, e35470.CrossRefGoogle ScholarPubMed
Xu, M, Jiang, Z, Huang, W, Yin, J, Ou, S, Jiang, Y, Meng, L, Cao, S, Yu, A, Cao, J and Shen, Y (2018) Altered gut microbiota composition in subjects infected with Clonorchis sinensis. Frontiers in Microbiology 9, 2292.CrossRefGoogle ScholarPubMed
Yang, CA, Liang, C, Lin, CL, Hsiao, CT, Peng, CT, Lin, HC and Chang, JG (2017) Impact of Enterobius vermicularis infection and mebendazole treatment on intestinal microbiota and host immune response. PLoS Neglected Tropical Diseases 11, e0005963.CrossRefGoogle ScholarPubMed
Zaiss, MM and Harris, NEL (2016) Interactions between the intestinal microbiome and helminth parasites. Parasite Immunology 38, 511.CrossRefGoogle ScholarPubMed
Supplementary material: File

Prommi et al. Supplementary Materials

Prommi et al. Supplementary Materials

Download Prommi et al. Supplementary Materials(File)
File 17.7 KB