Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-27T09:33:16.390Z Has data issue: false hasContentIssue false

Pinning down the role of common luminal intestinal parasitic protists in human health and disease – status and challenges

Published online by Cambridge University Press:  08 February 2019

Christen Rune Stensvold*
Affiliation:
Laboratory of Parasitology, Department of Bacteria, Parasites and Fungi, Statens Serum Institut, Artillerivej 5, DK–2300 Copenhagen S, Denmark
*
Author for correspondence: Christen Rune Stensvold, E-mail: [email protected]

Abstract

While some single-celled intestinal parasites are direct causes of diarrhoea and other types of intestinal pathology, the impact of other gut micro-eukaryotes on human health remains elusive. The fact that some common luminal intestinal parasitic protists (CLIPPs) have lately been found more often in healthy than in diseased individuals has fuelled the hypothesis that some parasites might in fact be protective against disease. To this end, the use of new DNA technologies has helped us investigate trans-kingdom relationships in the gut. However, research into these relationships is currently hampered by the limited data available on the genetic diversity within the CLIPPs genera, which results in limited efficacy of publicly available DNA sequence databases for taxonomic annotation of sequences belonging to the eukaryotic component of the gut microbiota. In this paper, I give a brief overview of the status on CLIPPs in human health and disease and challenges related to the mapping of intestinal eukaryotic diversity of the human gut.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2019 

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

Aguiar, JI, Gonçalves, AQ, Sodré, FC, Pereira, SOR, Bóia, MN, de Lemos, ER and Daher, RR (2007) Intestinal protozoa and helminths among Terena Indians in the State of Mato Grosso do Sul: high prevalence of Blastocystis hominis. Revista da Sociedade Brasileira de Medicina Tropical 40, 631634.Google Scholar
Alfellani, MA, Jacob, AS, Perea, NO, Krecek, RC, Taner-Mulla, D, Verweij, JJ, Levecke, B, Tannich, E, Clark, CG and Stensvold, CR (2013 a) Diversity and distribution of Blastocystis sp. subtypes in non-human primates. Parasitology 140, 966971.Google Scholar
Alfellani, MA, Taner-Mulla, D, Jacob, AS, Imeede, CA, Yoshikawa, H, Stensvold, CR and Clark, CG (2013 b) Genetic diversity of Blastocystis in livestock and zoo animals. Protist 164, 497509.Google Scholar
Andersen, LO and Stensvold, CR (2016) Blastocystis in health and disease: are we moving from a clinical to a public health perspective? Journal of Clinical Microbiology 54, 524528.Google Scholar
Andersen, LO, Bonde, I, Nielsen, HB and Stensvold, CR (2015) A retrospective metagenomics approach to studying Blastocystis. FEMS Microbiology Ecology 91, PubMed PMID: 26130823. doi: 10.1093/femsec/fiv072.Google Scholar
Auchtung, TA, Fofanova, TY, Stewart, CJ, Nash, AK, Wong, MC, Gesell, JR, Auchtung, JM, Ajami, NJ and Petrosino, JF (2018) Investigating colonization of the healthy adult gastrointestinal tract by fungi. mSphere 3, pii: e00092–18. doi: 10.1128/mSphere.00092-18.Google Scholar
Bates, ST, Clemente, JC, Flores, GE, Walters, WA, Parfrey, LW, Knight, R and Fierer, N (2013) Global biogeography of highly diverse protistan communities in soil. The ISME Journal 7, 652659.Google Scholar
Beghini, F, Pasolli, E, Truong, TD, Putignani, L, Cacciò, SM and Segata, N (2017) Large-scale comparative metagenomics of Blastocystis, a common member of the human gut microbiome. The ISME Journal 11, 28482863.Google Scholar
Bruijnesteijn van Coppenraet, LE, Wallinga, JA, Ruijs, GJ, Bruins, MJ and Verweij, JJ (2009) Parasitological diagnosis combining an internally controlled real-time PCR assay for the detection of four protozoa in stool samples with a testing algorithm for microscopy. Clinical Microbiology and Infection 15, 869874.Google Scholar
Cacciò, SM, Sannella, AR, Manuali, E, Tosini, F, Sensi, M, Crotti, D and Pozio, E (2012) Pigs as natural hosts of Dientamoeba fragilis genotypes found in humans. Emerging Infectious Diseases 18, 838841.Google Scholar
Cacciò, SM, Sannella, AR, Bruno, A, Stensvold, CR, David, EB, Guimarães, S, Manuali, E, Magistrali, C, Mahdad, K, Beaman, M, Maserati, R, Tosini, F and Pozio, E (2016) Multilocus sequence typing of Dientamoeba fragilis identified a major clone with widespread geographical distribution. International Journal for Parasitology 46, 793798.Google Scholar
Cani, PD (2018) Human gut microbiome: hopes, threats and promises. Gut 67, 17161725.Google Scholar
Chouari, R, Leonard, M, Bouali, M, Guermazi, S, Rahli, N, Zrafi, I, Morin, L and Sghir, A (2017) Eukaryotic molecular diversity at different steps of the wastewater treatment plant process reveals more phylogenetic novel lineages. World Journal of Microbiology and Biotechnology 33, 44.Google Scholar
Clark, CG (2000) Cryptic genetic variation in parasitic protozoa. Journal of Medical Microbiology 49, 489491.Google Scholar
Clark, CG and Stensvold, CR (2016) Blastocystis: isolation, xenic cultivation, and cryopreservation. Current Protocols in Microbiology 43, 20A.21.2120A.21.28.Google Scholar
Clark, CG, van der Giezen, M, Alfellani, MA and Stensvold, CR (2013) Recent developments in blastocystis research. Advances in Parasitology 82, 132.Google Scholar
Cociancic, P, Zonta, ML and Navone, GT (2018) A cross-sectional study of intestinal parasitoses in dogs and children of the periurban area of La Plata (Buenos Aires, Argentina): zoonotic importance and implications in public health. Zoonoses and Public Health 65, e44e53.Google Scholar
Constenla, M, Padrós, F and Palenzuela, O (2014) Endolimax piscium sp. nov. (Amoebozoa), causative agent of systemic granulomatous disease of cultured sole, Solea senegalensis Kaup. Journal of Fish Diseases 37, 229240.Google Scholar
Cristescu, ME (2014) From barcoding single individuals to metabarcoding biological communities: towards an integrative approach to the study of global biodiversity. Trends in Ecology & Evolution 29, 566571.Google Scholar
de Jong, MJ, Korterink, JJ, Benninga, MA, Hilbink, M, Widdershoven, J and Deckers-Kocken, JM (2014) Dientamoeba fragilis and chronic abdominal pain in children: a case-control study. Archives of Disease in Childhood 99, 11091113.Google Scholar
El Safadi, D, Gaayeb, L, Meloni, D, Cian, A, Poirier, P, Wawrzyniak, I, Delbac, F, Dabboussi, F, Delhaes, L, Seck, M, Hamze, M, Riveau, G and Viscogliosi, E (2014) Children of Senegal River Basin show the highest prevalence of Blastocystis sp. ever observed worldwide. BMC Infectious Diseases 14, 164.Google Scholar
Elsheikha, HM, Regan, CS and Clark, CG (2018) Novel entamoeba findings in nonhuman primates. Trends in Parasitology 34, 283294.Google Scholar
Faria, CP, Zanini, GM, Dias, GS, da Silva, S, de Freitas, MB, Almendra, R, Santana, P and Sousa, MD (2017) Geospatial distribution of intestinal parasitic infections in Rio de Janeiro (Brazil) and its association with social determinants. PLoS Neglected Tropical Diseases 11, e0005445.Google Scholar
Greigert, V, Abou-Bacar, A, Brunet, J, Nourrisson, C, Pfaff, AW, Benarbia, L, Pereira, B, Randrianarivelojosia, M, Razafindrakoto, JL, Solotiana Rakotomalala, R, Morel, E, Candolfi, E and Poirier, P (2018) Human intestinal parasites in Mahajanga, Madagascar: the kingdom of the protozoa. PLoS ONE 13, e0204576.Google Scholar
Hamad, I, Abou Abdallah, R, Ravaux, I, Mokhtari, S, Tissot-Dupont, H, Michelle, C, Stein, A, Lagier, JC, Raoult, D and Bittar, F (2018) Metabarcoding analysis of eukaryotic microbiota in the gut of HIV-infected patients. PLoS ONE 13, e0191913.Google Scholar
Heitlinger, E, Ferreira, SCM, Thierer, D, Hofer, H and East, ML (2017) The intestinal eukaryotic and bacterial biome of spotted hyenas: the impact of social status and age on diversity and composition. Frontiers in Cellular and Infection Microbiology 7, 262.Google Scholar
Higa, MG, Cardoso, WM, Weis, SMDS, França, AO, Pontes, ERJC, Silva, PVD, Oliveira, MP and Dorval, MEMC (2017) Intestinal parasitism among waste pickers in Mato Grosso do Sul, Midwest Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo 59, e87.Google Scholar
Holtman, GA, Kranenberg, JJ, Blanker, MH, Ott, A, Lisman-van Leeuwen, Y and Berger, MY (2017) Dientamoeba fragilis colonization is not associated with gastrointestinal symptoms in children at primary care level. Family Practice 34, 2529.Google Scholar
Jacob, AS, Busby, EJ, Levy, AD, Komm, N and Clark, CG (2016) Expanding the entamoeba universe: new hosts yield novel ribosomal lineages. Journal of Eukaryotic Microbiology 63, 6978.Google Scholar
Jeske, S, Bianchi, TF, Moura, MQ, Baccega, B, Pinto, NB, Berne, MEA and Villela, MM (2018) Intestinal parasites in cancer patients in the South of Brazil. Brazilian Journal of Biology 78, 574578.Google Scholar
Jokelainen, P, Hebbelstrup Jensen, B, Andreassen, BU, Petersen, AM, Röser, D, Krogfelt, KA, Nielsen, HV and Stensvold, CR (2017) Dientamoeba fragilis – a commensal in children in Danish day care centers. Journal of Clinical Microbiology 55, 17071713.Google Scholar
Jones, BM and Kustka, AB (2017) A quantitative SMRT cell sequencing method for ribosomal amplicons. Journal of Microbiological Methods 135, 7784.Google Scholar
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.Google Scholar
Krogsgaard, LR, Engsbro, AL, Stensvold, CR, Nielsen, HV and Bytzer, P (2015) The prevalence of intestinal parasites is not greater among individuals with irritable bowel syndrome: a population-based case-control study. Clinical Gastroenterology and Hepatology 13, 507513.e502Google Scholar
Krogsgaard, LR, Andersen, LO, Johannesen, TB, Engsbro, AL, Stensvold, CR, Nielsen, HV and Bytzer, P (2018) Characteristics of the bacterial microbiome in association with common intestinal parasites in irritable bowel syndrome. Clinical and Translational Gastroenterology 9, 161.Google Scholar
Laforest-Lapointe, I and Arrieta, MC (2018) Microbial eukaryotes: a missing link in gut microbiome studies. mSystems 3, pii: e00201–17.Google Scholar
Lukeš, J, Stensvold, CR, Jirků-Pomajbíková, K and Wegener Parfrey, L (2015) Are human intestinal eukaryotes beneficial or commensals? PLoS Pathogens 11, e1005039.Google Scholar
Maritz, JM, Rogers, KH, Rock, TM, Liu, N, Joseph, S, Land, KM and Carlton, JM (2017) An 18S rRNA workflow for characterizing protists in sewage, with a focus on zoonotic trichomonads. Microbial Ecology 74, 923936.Google Scholar
Masuda, A, Sumiyoshi, T, Ohtaki, T and Matsumoto, J (2018) Prevalence and molecular subtyping of Blastocystis from dairy cattle in Kanagawa, Japan. Parasitology International 67, 702705.Google Scholar
Matsubayashi, M, Shimada, Y, Li, YY, Harada, H and Kubota, K (2017) Phylogenetic diversity and in situ detection of eukaryotes in anaerobic sludge digesters. PLoS ONE 12, e0172888.Google Scholar
Matsunaga, K, Kubota, K and Harada, H (2014) Molecular diversity of eukaryotes in municipal wastewater treatment processes as revealed by 18S rRNA gene analysis. Microbes and Environments 29, 401407.Google Scholar
Mirjalali, H, Abbasi, MR, Naderi, N, Hasani, Z, Mirsamadi, ES, Stensvold, CR, Balaii, H, Asadzadeh Aghdaei, H and Zali, MR (2017) Distribution and phylogenetic analysis of Blastocystis sp. subtypes isolated from IBD patients and healthy individuals in Iran. European Journal of Clinical Microbiology & Infectious Diseases 36, 23352342.Google Scholar
Moon-van der Staay, SY, van der Staay, GW, Michalowski, T, Jouany, JP, Pristas, P, Javorský, P, Kišidayová, S, Varadyova, Z, McEwan, NR, Newbold, CJ, van Alen, T, de Graaf, R, Schmid, M, Huynen, MA and Hackstein, JH (2014) The symbiotic intestinal ciliates and the evolution of their hosts. European Journal of Protistology 50, 166173.Google Scholar
Moreno, AM, Matz, C, Kjelleberg, S and Manefield, M (2010) Identification of ciliate grazers of autotrophic bacteria in ammonia-oxidizing activated sludge by RNA stable isotope probing. Appl Environ Microbiol 76, 22032211.Google Scholar
Morton, ER, Lynch, J, Froment, A, Lafosse, S, Heyer, E, Przeworski, M, Blekhman, R and Ségurel, L (2015) Variation in Rural African gut microbiota is strongly correlated with colonization by entamoeba and subsistence. PLoS Genetics 11, e1005658.Google Scholar
Moura, RGF, Oliveira-Silva, MB, Pedrosa, AL, Nascentes, GAN and Cabrine-Santos, M (2018) Occurrence of Blastocystis spp. in domestic animals in Triângulo Mineiro area of Brazil. Revista da Sociedade Brasileira de Medicina Tropical 51, 240243.Google Scholar
Munasinghe, VS, Vella, NG, Ellis, JT, Windsor, PA and Stark, D (2013) Cyst formation and faecal-oral transmission of Dientamoeba fragilis – the missing link of the life cycle of an emering pathogen. International Journal for Parasitology 43, 879883.Google Scholar
Myer, PR, Kim, M, Freetly, HC and Smith, TP (2016) Metagenomic and near full-length 16S rRNA sequence data in support of the phylogenetic analysis of the rumen bacterial community in steers. Data in Brief 8, 10481053.Google Scholar
Nakano, K, Shiroma, A, Shimoji, M, Tamotsu, H, Ashimine, N, Ohki, S, Shinzato, M, Minami, M, Nakanishi, T, Teruya, K, Satou, K and Hirano, T (2017) Advantages of genome sequencing by long-read sequencer using SMRT technology in medical area. Human Cell 30, 149161.Google Scholar
Navarro, C, Domínguez-Márquez, MV, Garijo-Toledo, MM, Vega-García, S, Fernández-Barredo, S, Pérez-Gracia, MT, García, A, Borrás, R and Gómez-Muñoz, MT (2008) High prevalence of Blastocystis sp. in pigs reared under intensive growing systems: frequency of ribotypes and associated risk factors. Veterinary Parasitology 153, 347358.Google Scholar
Neres-Norberg, A, Guerra-Sanches, F, Blanco Moreira-Norberg, PR, Madeira-Oliveira, JT, Santa-Helena, AA and Serra-Freire, NM (2014) [Intestinal Parasitism in Terena Indigenous People of the Province of Mato Grosso do Sul, Brazil]. Revista de Salud Publica (Bogota) 16, 859870.Google Scholar
Ögren, J, Dienus, O, Löfgren, S, Einemo, IM, Iveroth, P and Matussek, A (2015) Dientamoeba fragilis prevalence coincides with gastrointestinal symptoms in children less than 11 years old in Sweden. European Journal of Clinical Microbiology & Infectious Diseases 34, 19951998.Google Scholar
Ohkuma, M (2008) Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends in Microbiology 16, 345352.Google Scholar
Oliverio, AM, Power, JF, Washburne, A, Cary, SC, Stott, MB and Fierer, N (2018) The ecology and diversity of microbial eukaryotes in geothermal springs. The ISME Journal 12, 19181928.Google Scholar
Orr, RJS, Zhao, S, Klaveness, D, Yabuki, A, Ikeda, K, Makoto, WM and Shalchian-Tabrizi, K (2018) Enigmatic Diphyllatea eukaryotes: culturing and targeted PacBio RS amplicon sequencing reveals a higher order taxonomic diversity and global distribution. BMC Evolutionary Biology 18, 115.Google Scholar
Pakandl, M (1991) Occurrence of Blastocystis sp. in pigs. Folia Parasitologica (Praha) 38, 297301.Google Scholar
Parfrey, LW, Walters, WA and Knight, R (2011) Microbial eukaryotes in the human microbiome: ecology, evolution, and future directions. Frontiers in Microbiology 2, 153.Google Scholar
Peek, R, Reedeker, FR and van Gool, T (2004) Direct amplification and genotyping of Dientamoeba fragilis from human stool specimens. Journal of Clinical Microbiology 42, 631635.Google Scholar
Petersen, AM, Stensvold, CR, Mirsepasi, H, Engberg, J, Friis-Møller, A, Porsbo, LJ, Hammerum, AM, Nordgaard-Lassen, I, Nielsen, HV and Krogfelt, KA (2013) Active ulcerative colitis associated with low prevalence of Blastocystis and Dientamoeba fragilis infection. Scandinavian Journal of Gastroenterology 48, 638639.Google Scholar
Poulsen, CS and Stensvold, CR (2016) Systematic review on Endolimax nana: a less well studied intestinal ameba. Tropical Parasitology 6, 829.Google Scholar
Poulsen, CS, Efunshile, AM, Nelson, JA and Stensvold, CR (2016) Epidemiological aspects of Blastocystis colonization in children in Ilero, Nigeria. American Journal of Tropical Medicine and Hygiene 95, 175179.Google Scholar
Powers, JG, Weigman, VJ, Shu, J, Pufky, JM, Cox, D and Hurban, P (2013) Efficient and accurate whole genome assembly and methylome profiling of E. coli. BMC Genomics 14, 675.Google Scholar
Ramirez, JD, Sanchez, LV, Bautista, DC, Corredor, AF, Florez, AC and Stensvold, CR (2014) Blastocystis subtypes detected in humans and animals from Colombia. Infection Genetics and Evolution 22, 223228.Google Scholar
Rene, BA, Stensvold, CR, Badsberg, JH and Nielsen, HV (2009) Subtype analysis of Blastocystis isolates from Blastocystis cyst excreting patients. American Journal of Tropical Medicine and Hygiene 80, 588592.Google Scholar
Rosenberg, K, Bertaux, J, Krome, K, Hartmann, A, Scheu, S and Bonkowski, M (2009) Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. The ISME Journal 3, 675684.Google Scholar
Roser, D, Simonsen, J, Nielsen, HV, Stensvold, CR and Molbak, K (2013) Dientamoeba fragilis in Denmark: epidemiological experience derived from four years of routine real-time PCR. European Journal of Clinical Microbiology & Infectious Diseases 32, 13031310.Google Scholar
Rossen, NG, Bart, A, Verhaar, N, van Nood, E, Kootte, R, de Groot, PF, D'Haens, GR, Ponsioen, CY and van Gool, T (2015) Low prevalence of Blastocystis sp. in active ulcerative colitis patients. European Journal of Clinical Microbiology & Infectious Diseases 34, 10391044.Google Scholar
Royer, TL, Gilchrist, C, Kabir, M, Arju, T, Ralston, KS, Haque, R, Clark, CG and Petri, WA (2012) Entamoeba bangladeshi nov. sp., Bangladesh. Emerging Infectious Diseases 18, 15431545.Google Scholar
Ruaux, CG and Stang, BV (2014) Prevalence of blastocystis in shelter-resident and client-owned companion animals in the US Pacific Northwest. PLoS ONE 9, e107496.Google Scholar
Růžková, J, Květoňová, D, Jirků, M, Lhotská, Z, Stensvold, CR, Parfrey, LW and Jirků Pomajbíková, K (2018) Evaluating rodent experimental models for studies of Blastocystis ST1. Experimental Parasitology 191, 5561.Google Scholar
Salehi, R, Haghighi, A, Stensvold, CR, Kheirandish, F, Azargashb, E, Raeghi, S, Kohansal, C and Bahrami, F (2017) Prevalence and subtype identification of. Gastroenterology and Hepatology From Bed To Bench 10, 235241.Google Scholar
Scanlan, PD, Stensvold, CR, Rajilić-Stojanović, M, Heilig, HG, De Vos, WM, O'Toole, PW and Cotter, PD (2014) The microbial eukaryote Blastocystis is a prevalent and diverse member of the healthy human gut microbiota. FEMS Microbiology Ecology 90, 326330.Google Scholar
Scanlan, PD, Hill, CJ, Ross, RP, Ryan, CA, Stanton, C and Cotter, PD (2018) The intestinal protist Blastocystis is not a common member of the healthy infant gut microbiota in a Westernized country (Ireland). Parasitology 145, 12741278.Google Scholar
Silberman, JD, Clark, CG, Diamond, LS and Sogin, ML (1999) Phylogeny of the genera Entamoeba and Endolimax as deduced from small-subunit ribosomal RNA sequences. Molecular Biology and Evolution 16, 17401751.Google Scholar
Stark, D, Beebe, N, Marriott, D, Ellis, J and Harkness, J (2005 a) Detection of Dientamoeba fragilis in fresh stool specimens using PCR. International Journal for Parasitology 35, 5762.Google Scholar
Stark, D, Beebe, N, Marriott, D, Ellis, J and Harkness, J (2005 b) Prospective study of the prevalence, genotyping, and clinical relevance of Dientamoeba fragilis infections in an Australian population. Journal of Clinical Microbiology 43, 27182723.Google Scholar
Stark, D, Beebe, N, Marriott, D, Ellis, J and Harkness, J (2006) Evaluation of three diagnostic methods, including real-time PCR, for detection of Dientamoeba fragilis in stool specimens. Journal of Clinical Microbiology 44, 232235.Google Scholar
Stark, D, Phillips, O, Peckett, D, Munro, U, Marriott, D, Harkness, J and Ellis, J (2008) Gorillas are a host for Dientamoeba fragilis: an update on the life cycle and host distribution. Veterinary Parasitology 151, 2126.Google Scholar
Stark, D, Garcia, LS, Barratt, JL, Phillips, O, Roberts, T, Marriott, D, Harkness, J and Ellis, JT (2014) Description of Dientamoeba fragilis cyst and precystic forms from human samples. Journal of Clinical Microbiology 52, 26802683.Google Scholar
Stark, D, Barratt, J, Chan, D and Ellis, JT (2016) Dientamoeba fragilis, the neglected trichomonad of the human bowel. Clinical Microbiology Reviews 29, 553580.Google Scholar
Stensvold, CR and Clark, CG (2016) Current status of Blastocystis: a personal view. Parasitology International 65, 763771.Google Scholar
Stensvold, CR and Nielsen, HV (2012) Comparison of microscopy and PCR for detection of intestinal parasites in Danish patients supports an incentive for molecular screening platforms. Journal of Clinical Microbiology 50, 540541.Google Scholar
Stensvold, CR and van der Giezen, M (2018) Associations between Gut Microbiota and common luminal intestinal parasites. Trends in Parasitology 34, 369377.Google Scholar
Stensvold, CR, Lebbad, M and Clark, CG (2010) Genetic characterisation of uninucleated cyst-producing Entamoeba spp. from ruminants. International Journal for Parasitology 40, 775778.Google Scholar
Stensvold, CR, Alfellani, M and Clark, CG (2011a) Levels of genetic diversity vary dramatically between Blastocystis subtypes. Infection Genetics and Evolution 12, 263273.Google Scholar
Stensvold, CR, Lebbad, M and Verweij, JJ (2011b) The impact of genetic diversity in protozoa on molecular diagnostics. Trends in Parasitology 27, 5358.Google Scholar
Stensvold, CR, Lebbad, M, Victory, EL, Verweij, JJ, Tannich, E, Alfellani, M, Legarraga, P and Clark, CG (2011c) Increased sampling reveals novel lineages of Entamoeba: consequences of genetic diversity and host specificity for taxonomy and molecular detection. Protist 162, 525541.Google Scholar
Stensvold, CR, Lebbad, M and Clark, CG (2012) Last of the human protists: the phylogeny and genetic diversity of iodamoeba. Molecular Biology and Evolution 29, 3942.Google Scholar
Stensvold, CR, Clark, CG and Röser, D (2013) Limited intra-genetic diversity in Dientamoeba fragilis housekeeping genes. Infection Genetics and Evolution 18, 284286.Google Scholar
Stensvold, CR, Winiecka-Krusnell, J, Lier, T and Lebbad, M (2018) Evaluation of a PCR method for detection of Entamoeba polecki, with an overview of Its molecular epidemiology. Journal of Clinical Microbiology 56, pii: e00154–18.Google Scholar
ten Hove, R, Schuurman, T, Kooistra, M, Möller, L, van Lieshout, L and Verweij, JJ (2007) Detection of diarrhoea-causing protozoa in general practice patients in The Netherlands by multiplex real-time PCR. Clinical Microbiology and Infection 13, 10011007.Google Scholar
Udonsom, R, Prasertbun, R, Mahittikorn, A, Mori, H, Changbunjong, T, Komalamisra, C, Pintong, AR, Sukthana, Y and Popruk, S (2018) Blastocystis infection and subtype distribution in humans, cattle, goats, and pigs in central and western Thailand. Infection Genetics and Evolution 65, 107111.Google Scholar
Veira, DM (1986) The role of ciliate protozoa in nutrition of the ruminant. Journal of Animal Science 63, 15471560.Google Scholar
Verweij, JJ (2014) Application of PCR-based methods for diagnosis of intestinal parasitic infections in the clinical laboratory. Parasitology 141, 18631872.Google Scholar
Verweij, JJ and Stensvold, CR (2014) Molecular testing for clinical diagnosis and epidemiological investigations of intestinal parasitic infections. Clinical Microbiology Reviews 27, 371418.Google Scholar
Verweij, JJ and van Lieshout, L (2011) Intestinal parasitic infections in an industrialized country; a new focus on children with better DNA-based diagnostics. Parasitology 138, 14921498.Google Scholar
Verweij, JJ, Polderman, AM and Clark, CG (2001) Genetic variation among human isolates of uninucleated cyst-producing entamoeba species. Journal of Clinical Microbiology 39, 16441646.Google Scholar
Verweij, JJ, Mulder, B, Poell, B, van Middelkoop, D, Brienen, EA and van Lieshout, L (2007) Real-time PCR for the detection of Dientamoeba fragilis in fecal samples. Molecular and Cellular Probes 21, 400404.Google Scholar
Wang, W, Owen, H, Traub, RJ, Cuttell, L, Inpankaew, T and Bielefeldt-Ohmann, H (2014) Molecular epidemiology of Blastocystis in pigs and their in-contact humans in Southeast Queensland, Australia, and Cambodia. Veterinary Parasitology 203, 264269.Google Scholar
Wilcox, JJS and Hollocher, H (2018) Unprecedented symbiont eukaryote diversity Is governed by internal trophic webs in a wild Non-human primate. Protist 169, 307320.Google Scholar
Xiong, J, Yu, W, Dai, W, Zhang, J, Qiu, Q and Ou, C (2018) Quantitative prediction of shrimp disease incidence via the profiles of gut eukaryotic microbiota. Applied Microbiology and Biotechnology 102, 33153326.Google Scholar
Yoshikawa, H, Koyama, Y, Tsuchiya, E and Takami, K (2016) Blastocystis phylogeny among various isolates from humans to insects. Parasitology International 65, 750759.Google Scholar
Yu, Y, Lee, C, Kim, J and Hwang, S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnology and Bioengineering 89, 670679.Google Scholar