Cyst detection and viability assessment of Balantioides coli in environmental samples: Current status and future needs

Adhikari, 2013, Prevalence of Buxtonella sulcata in water buffaloes and cows in Chitwan Valley, southern Nepal, Japanese J. Vet. Parasitol., 11, 55 Agobian, 2013, Contaminación por enteroparásitos en repollos comercializados en los estados Lara, Yaracuy y Portuguesa, Rev. Venez. Salud Pública, 1, 7 Ajeagah, 2014, Study of the influence of environmental factors on the occurrence of Balantidium coli cysts in an urban aquatic system in Cameroon, J. Ecol. Nat. Environ., 6, 190, 10.5897/JENE2014.0451 Ajitha, 2020, Study on parasitic contamination of common edible fruits and vegetables sold in local markets of Tiruchirappalli, South India, Indian J. Microbiol. Res., 7, 362, 10.18231/j.ijmr.2020.065 Akoachere, 2018, Bacterial and parasitic contaminants of salad vegetables sold in markets in Fako division, Cameroon and evaluation of hygiene and handling practices of vendors, BMC Res. Notes, 11, 100, 10.1186/s13104-018-3175-2 Alade, 2013, Prevalence of intestinal parasites in vegetables sold in Ilorin, Nigeria, J. Agric. Environ. Sci, 13, 1275 Alemu, 2019, Parasitic contamination of vegetables marketed in Arba Minch town, southern Ethiopia, BMC Infect. Dis., 19, 1, 10.1186/s12879-019-4020-5 Al-Sanabani, 2016, Prevalence of intestinal parasites in fresh leafy vegetables in some farms at Dhamar city, Yemen, Int. J. Med. Res., 1, 7 Al-Tufaili, 2014, Investigation of parasitic contamination in Kufa river water-Al-Najaf province, Al-Kufa Univ. J. Biol., 6, 11 Amaechi, 2016, Prevalence of parasitic contamination of salad vegetables in Ilorin, North Central, Nigeria, Momona Ethiop. J. Sci., 8, 136, 10.4314/mejs.v8i2.3 Amin, 1988, Pathogenic Micro-organisms and Helminths in sewage products, Arabian gulf, country of Bahrain, Am. J. Public Health, 78, 314, 10.2105/AJPH.78.3.314 Amoah, 2017, Detection and quantification of soil-transmitted helminths in environmental samples: a review of current state-of-the-art and future perspectives, Acta Trop., 169, 187, 10.1016/j.actatropica.2017.02.014 Auad, 2019, Food trucks: assessment of an evaluation instrument designed for the prevention of foodborne diseases, Nutrients, 11, 1 Ayaz, 2011, Prevalence of zoonotic parasites in drinking water of three districts of Khyber Pakhtunkhwa Province, Pakistan, Pakistan J. Life Soc. Sci., 9, 67 Baldursson, 2011, Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update 2004-2010, Water Res., 45, 6603, 10.1016/j.watres.2011.10.013 Ballweber, 2014, American association of veterinary parasitologists’ review of veterinary fecal flotation methods and factors influencing their accuracy and use - is there really one best technique?, Vet. Parasitol., 204, 73, 10.1016/j.vetpar.2014.05.009 Bareja, 2015, The simplest technique for cultivation and maintenance of Balantidium coli, Int. J. Heal. Allied Sci., 4, 218, 10.4103/2278-344X.167650 Benčaťová, 2017, A study on resting cysts of an oxytrichid soil ciliate, Rigidohymena quadrinucleata (Dragesco and Njine, 1971) Berger, 2011 (Ciliophora, Hypotrichia), including notes on its encystation and excystation process, Acta Protozool., 56, 77 Bouwknegt, 2018, Prioritisation of food-borne parasites in Europe, 2016, Eurosurveillance, 23, 1, 10.2807/1560-7917.ES.2018.23.9.17-00161 Bridle, 2014, Sample processing, 1 Chalmers, 2014, Balantidium coli, 277 Chalmers, 2020, Parasite detection in food: current status and future needs for validation, Trends Food Sci. Technol., 99, 337, 10.1016/j.tifs.2020.03.011 Chao, 2006, A statistical approach to estimate soil ciliate diversity and distribution based on data from five continents, Oikos, 114, 479, 10.1111/j.2006.0030-1299.14814.x Charitha, 2015, Contamination of soil with parasitic forms in urban and rural areas of Andhra Pradesh, India, J. Parasitol. Phot., 105, 227 Clark, 2002, Methods for cultivation of luminal parasitic protists of clinical importance, Clin. Microbiol. Rev., 10.1128/CMR.15.3.329-341.2002 Collender, 2015, Methods for quantification of soil-transmitted helminths in environmental media: current techniques and recent advances, Trends Parasitol., 31, 625, 10.1016/j.pt.2015.08.007 Cork, 2011, Globalization of the food supply and the spread of disease, 1 da Silva Barbosa, 2015, Isolation and maintenance of Balantidium coli (Malmsteim, 1857) cultured from fecal samples of pigs and non-human primates, Vet. Parasitol., 210, 240, 10.1016/j.vetpar.2015.03.030 da Silva Barbosa, 2016, Comparison of five parasitological techniques for laboratory diagnosis of Balantidium coli cysts, Rev. Bras. Parasitol. Vet., 25, 286, 10.1590/S1984-29612016044 da Silva Barbosa, 2018, Comparative study of three xenic media culture for cultivation of Balantidium coli strains, Brazil. J. Vet. Parasitol., 27, 19, 10.1590/s1984-29612017075 da Silva Barbosa, 2018, Balantioides coli: morphological and ultrastructural characteristics of pig and non-human primate isolates, Acta Parasitol., 63, 287, 10.1515/ap-2018-0033 Daminabo, 2020, Prevalence of intestinal parasites from abattoir effluents in Jos Metropolis, Nigeria, Int. J. Photochem. Photobiol., 4, 1, 10.11648/j.ijpp.20200401.11 Dawson, 2005, Foodborne protozoan parasites, Int. J. Food Microbiol., 103, 207, 10.1016/j.ijfoodmicro.2004.12.032 Dixon, 2015, Transmission dynamics of foodborne parasites on fresh produce, 317 dos Carolino Fiorido, 2020, Análise parasitológica de frutas consumidas com casca, comercializadas em supermercados de uma cidade do sudeste do Brasil, Heal. Biosci., 1, 63 Efstratiou, 2017, Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update 2011–2016, Water Res., 114, 14, 10.1016/j.watres.2017.01.036 Ensink, 2007, Wastewater-irrigated vegetables: market handling versus irrigation water quality, Tropical Med. Int. Health, 12, 2, 10.1111/j.1365-3156.2007.01935.x Ericksen, 1986, Methods to identify waterborne pathogens and indicator organisms, 195 Erickson, 2006, Inactivation of protozoan parasites in food, water, and environmental systems, J. Food Prot., 69, 2786, 10.4315/0362-028X-69.11.2786 Etewa, 2016, Geohelminths distribution as affected by soil properties, physicochemical factors and climate in Sharkyia governorate Egypt, J. Parasit. Dis., 40, 496, 10.1007/s12639-014-0532-5 Etewa, 2017, Parasitic contamination of commonly consumed fresh vegetables and fruits in some rural areas of Sharkyia governorate, Egypt, Afro-Egypt. J. Infect. Endem. Dis., 7, 192 Ferreira Martins, 2017, Métodos parasitológicos aplicados em espécimes de solo e água em setores do município de Guaraí/TO, Scire Salut., 7, 32, 10.6008/SPC2236-9600.2017.002.0004 Food and Agriculture Organization of the United Nations, World Health Organization, 2014, 23 Gabaldon, 1935, Balantidium coli : quantitative studies in experimental infections and variations in infectiousness for rats, J. Parasitol., 21, 386, 10.2307/3271950 García-Rodríguez, 2020, Genetic identification of the ciliates from greater rheas (Rhea americana) and lesser rheas (Rhea pennata) as Balantioides coli, Parasitol. Res., 119, 755, 10.1007/s00436-019-06559-5 Gérard, 2019, Inactivation of parasite transmission stages: efficacy of treatments on foods of non-animal origin, Trends Food Sci. Technol., 91, 12, 10.1016/j.tifs.2019.06.015 Gomez Hinojosa, 2019, Balantidiasis colónica: reporte de un caso fatal y revisión de la literatura, Rev. Gastroenterol. Peru, 39, 284 Grim, 2015, Light microscopic morphometrics, ultrastructure, and molecular phylogeny of the putative pycnotrichid ciliate, Buxtonella sulcata, Eur. J. Protistol., 51, 425, 10.1016/j.ejop.2015.06.003 Gutiérrez, 2001, Ciliate cryptobiosis: a microbial strategy against environmental starvation, Int. Microbiol., 4, 151, 10.1007/s10123-001-0030-3 Hassan, 2012, Parasitological contamination of freshly eaten vegetables collected from local markets in Alexandria, Egypt: a preliminary study, Food Control, 26, 500, 10.1016/j.foodcont.2012.01.033 Herman, 2015, Outbreaks attributed to fresh leafy vegetables, United States, 1973-2012, Epidemiol. Infect., 143, 3011, 10.1017/S0950268815000047 Hoffman, 2009, Prioritizing pathogens for potential future regulation in drinking water, Environ. Sci. Technol., 43, 5165, 10.1021/es803532k Karaman, 2017, The Protozoa and helminths in the water of Terme and Kocaman Boroughs of Samsun Province, J. Turgut Ozal Med. Cent., 24, 472 Karanis, 2002, Evaluation of three flocculation methods for the purification of Cryptosporidium parvum oocysts from water samples, Lett. Appl. Microbiol., 34, 444, 10.1046/j.1472-765X.2002.01121.x Karanis, 2007, Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt, J. Water Health, 5, 1, 10.2166/wh.2006.002 Kaur, 2019, Encystment and excystment in ciliated protists: multidimensional approach, Curr. Sci., 117, 198, 10.18520/cs/v117/i2/198-203 Khanum, 2012, Protozoan parasites in a wastewater treatment plant of Bangladesh, Univ. J. Zool. Rajshahi Univ., 31, 5, 10.3329/ujzru.v31i0.15372 Kourenti, 2003, Development and application of different methods for the detection of toxoplasma gondii in water, Appl. Environ. Microbiol., 69, 102, 10.1128/AEM.69.1.102-106.2003 Kudah, 2018, Parasitic contamination of commonly consumed vegetables in two markets in Ghana, Ghana Med. J., 52, 88, 10.4314/gmj.v52i2.5 Li, 2020, Detection of human intestinal protozoan parasites in vegetables and fruits: a review, Parasit. Vectors, 13, 380, 10.1186/s13071-020-04255-3 Little, 1931, A note on Balantidium coli, J. R. Army Med. Corps, 56, 298 López Arias, 2017, Development of a PCR assay for identification of Neobalantidium coli (Pomajbíková et al., 2013) in Argentina, Vet. Parasitol. Reg. Stud. Rep., 10, 114 Lora-Suarez, 2016, Detection of protozoa in water samples by formalin/ether concentration method, Water Res., 100, 377, 10.1016/j.watres.2016.05.038 Manser, 2016, Faecal parasitology: concentration methodology needs to be better standardised, PLoS Negl. Trop. Dis., 10, 10.1371/journal.pntd.0004579 Matini, 2017, The parasitic contamination of farm vegetables in Asadabad City, West of Iran, in 2014, Avicenna J. Clin. Microbiol. Infect., 4 McDonald, 1922, On Balantidium coli (Malmsten) and Balantidium suis (sp. nov.), with an account of their neuro-motor apparatus, Univ. Calif. Publ. Zool., 20, 243 Milinovich, 2011, Manure as a source of zoonotic pathogens, 59 Morais da Silva, 2014, Detection of intestinal parasites on field-grown strawberries in the Federal District of Brazil, Rev. Soc. Bras. Med. Trop., 47, 801, 10.1590/0037-8682-0044-2014 Moreno, 2018, Multiple identification of most important waterborne protozoa in surface water used for irrigation purposes by 18S rRNA amplicon-based metagenomics, Int. J. Hyg. Environ. Health, 221, 102, 10.1016/j.ijheh.2017.10.008 Mukhtar, 2016, Role of vegetables in the transmission of intestinal parasites in Khartoum central market, Khartoum State, Sudan, Eur. Acad. Res., 3, 11825 Nazemi, 2012, Parasitic contamination of raw vegetables in Shahroud, Semnan, Zahedan J. Res. Med. Sci., 14, 84 Nsoh, 2016, Prevalence, characteristics and correlates of enteric pathogenic protozoa in drinking water sources in Molyko and Bomaka, Cameroon: a cross-sectional study, BMC Microbiol., 16, 268, 10.1186/s12866-016-0890-5 Ogunremi, 2017, Human enteric parasitic pathogens in fresh fruits and vegetables consumed in Ile-Ife, Osun State. Food Sci. Qual. Manag., 66, 34 Ordoñez, 2018, Parasite contamination of freshly harvested vegetables from selected organic and conventional farms in the Philippines, Pertanika J. Trop. Agric. Sci., 41, 1741 Orlandi, 2002, Parasites and the food supply, Food Technol., 56, 72 Oyibo, 2016, Evaluation of parasites of medical importance in drinking water sources in Okura District, Dekina Local Gobernment, Kogi State, Nigeria, Int. J. Dev. Res., 6, 7290 Pires, 2009, Attributing the human disease burden of foodborne infections to specific sources, Foodborne Pathog. Dis., 6, 417, 10.1089/fpd.2008.0208 Pires, 2012, Attributing human foodborne illness to food sources and water in Latin America and the Caribbean using data from outbreak investigations, Int. J. Food Microbiol., 152, 129, 10.1016/j.ijfoodmicro.2011.04.018 Poma, 2012, Towards a rational strategy for monitoring of microbiological quality of ambient waters, Sci. Total Environ., 433, 98, 10.1016/j.scitotenv.2012.06.019 Pomajbíková, 2010, Discrepancies in the occurrence of Balantidium coli between wild and captive African great apes, J. Parasitol., 96, 1139, 10.1645/GE-2433.1 Pomajbíková, 2013, Novel insights into the genetic diversity of Balantidium and Balantidium-like cyst-forming ciliates, PLoS Negl. Trop. Dis., 7, 10.1371/journal.pntd.0002140 Ponce-Gordo, 2021, Balantioides coli, Res. Vet. Sci., 135, 424, 10.1016/j.rvsc.2020.10.028 Ponce-Gordo, 2017, Balantidium coli, 14 Ponce-Gordo, 2008, Tentative identification of the species of Balantidium from ostriches (Struthio camelus) as Balantidium coli-like by analysis of polymorphic DNA, Vet. Parasitol., 157, 41, 10.1016/j.vetpar.2008.06.024 Ponce-Gordo, 2011, Genetic heterogeneity in internal transcribed spacer genes of Balantidium coli (Litostomatea, Ciliophora), Protist, 162, 774, 10.1016/j.protis.2011.06.008 Rees, 1927, Balantidia from pigs and guinea-pigs: their viability, cyst production and cultivation, Science (80-. ), 66, 89, 10.1126/science.66.1699.89 Robertson, 2014, Protozoan parasites: A plethora of potentially foodborne pathogens, 169 Rodrigues Maldonade, 2019, Good manufacturing practices of minimally processed vegetables reduce contamination with pathogenic microorganisms, Rev. Inst. Med. Trop. Sao Paulo, 61 Rosado-García, 2017, Water-borne protozoa parasites: the Latin American perspective, Int. J. Hyg. Environ. Health, 220, 783, 10.1016/j.ijheh.2017.03.008 Rousseau, 2018, Assessing viability and infectivity of foodborne and waterborne stages (cysts/oocysts) of Giardia duodenalis, Cryptosporidium spp., and Toxoplasma gondii: a review of methods, Parasite, 25 Schaefer, 2004, Inactivation and removal of enteric protozoa in water, 117 Schumaker, 1930, Experimental infection of rats with the Balantidium from the pig, Science (80-. ), 70, 384, 10.1126/science.70.1816.384 Schuster, 2004, Amebae and ciliated protozoa as causal agents of waterborne zoonotic disease, Vet. Parasitol., 126, 91, 10.1016/j.vetpar.2004.09.019 Sena Barnabé, 2010, Análisis comparativo de los métodos para la detección de parásitos en las hortalizas para el consumo humano, Rev. Cuba. Med. Trop. Trop, 62, 21 Shah, 2016, Assessment of safety of drinking water in tank district: an empirical study of water-borne diseases in rural Khyber Pakhtunkhwa, Pakistan, Int. J. Environ. Sci., 6, 418 Shikara, 2019, Evaluation of some Physico-chemical and detection of parasites in sediment of Hamrin Lake, Iraqi J. Sci. Technol., 10, 96 Smith, 1998, Detection of parasites in the environment, Parasitology, 117, S113, 10.1017/S0031182099004898 Soares, 2020, A historical review of the techniques of recovery of parasites for their detection in human stools, Rev. Soc. Bras. Med. Trop., 53, 10.1590/0037-8682-0535-2019 Tobón, 2018, Procedure optimization for concentration and detection of protozoa and helminths in great volumes of water, Rev. Cubana Med. Trop., 70, 71 Traub, 2015, Laboratory diagnostic methods, 403 Verni, 2011, Resting cysts: a survival strategy in protozoa ciliophora, Ital. J. Zool., 78, 134, 10.1080/11250003.2011.560579 Viezzer Bianchi, 2019, Fatal parasite-induced enteritis and typhlocolitis in horses in southern Brazil, Rev. Bras. Parasitol. Vet., 28, 443, 10.1590/s1984-29612019056 Walker, 1913, Experimental balantidiasis, Philipp. J. Sci. Sect. B. Trop. Med., 8, 333 Walzer, 1973, Balantidiasis outbreak in Truk, Am. J. Trop. Med. Hyg., 22, 33, 10.4269/ajtmh.1973.22.33 World Health Organization, 2017 Yan, 2018, First molecular identification of Buxtonella ciliates from captive-bred mangabeys (Cercocebus torquatus) from China, Parasitol. Res., 117, 3753, 10.1007/s00436-018-6075-4 Yan, 2021, Modified DMEM xenic culture medium for propagation, isolation and maintenance of Balantioides coli, Acta Trop., 214, 10.1016/j.actatropica.2020.105762 Young, 1950, Attempts to transmit human Balantidium coli, Am. J. Trop. Med., s1-30, 71, 10.4269/ajtmh.1950.s1-30.71 Zhang, 2013, Detecting Cryptosporidium parvum and Giardia lamblia by coagulation concentration and real-time PCR quantification, Front. Environ. Sci. Eng., 7, 49, 10.1007/s11783-012-0455-2