Molecular detection and characterization of Cryptosporidium spp. in the sewage-contaminated rivers entering Bandar-e Anzali Lagoon in Guilan Province, Iran

Document Type : Original Article

Author

1 Cellular and Molecular Research Center, Faculty of Medicine, Guilan University of Medical Sciences, Rasht, Iran

2 Department of Parasitology, Faculty of Medicine, Guilan University of Medical Sciences, Rasht, Iran

3 Medical Biotechnology Research Center, Guilan University of Medical Sciences, Rasht, Iran

Abstract

Waterborne cryptosporidiosis in river water is considered to be an important source of Cryptosporidium oocysts in most developing countries across the world. In the present study, 20 water samples were collected from Zarjoob and Goharrood rivers contaminated with wastewater in the province of Guilan, Iran. The samples were filtrated through a membrane filter (pore size: 1.2 μm), then the sucrose clarification and molecular genotyping methods were also carried out. In total, 12 out of 20 water samples were positive for Cryptosporidium species based on the 18S RNA-based polymerase chain reaction (PCR) and sequencing techniques. In addition, C. parvum, C. muris, C. homnis, and C. canis were detected in the water samples studied. According to the results, river water resources were polluted with the pathogenic species of Cryptosporidium with human and animal sources, which increased the potential risk of waterborne cryptosporidiosis. Moreover, the long-term use of sewage-contaminated river water to irrigate crops and agriculture farms could be a major threat to local residents.

Keywords


1.     Feng Y, Li N, Duan L, Xiao L. Cryptosporidium genotype and subtype distribution in raw wastewater in Shanghai, China: Evidence for possible unique Cryptosporidium hominis transmission. J Clin Microbiol 2009; 47(1): 153-7.
2.         Imre K, Morar A, Ilie MS, Plutzer J, Imre M, Emil T, et al. Survey of the occurrence and human infective potential of Giardia duodenalis and Cryptosporidium spp. in wastewater and different surface water sources of western Romania. Vector Borne Zoonotic Dis 2017; 17(10): 685-91.
3.         Efstratiou A, Ongerth J, Karanis P. Evolution of monitoring for Giardia and Cryptosporidium in water. Water Res 2017; 123: 96-112.
4.         Lu P, Amburgey JE, Hill VR, Murphy JL, Schneeberger CL, Arrowood MJ, et al. Removals of cryptosporidium parvum oocysts and cryptosporidium-sized polystyrene microspheres from swimming pool water by diatomaceous earth filtration and perlite-sand filtration. J Water Health 2017; 15(3): 374-84.
5.         Mahmoudi MR, Ongerth JE, Karanis P. Cryptosporidium and cryptosporidiosis: The Asian perspective. Int J Hyg Environ Health 2017; 220(7): 1098-109.
6.         Karanis P, Kourenti C, Smith H. Waterborne transmission of protozoan parasites: A worldwide review of outbreaks and lessons learnt. J Water Health 2007; 5(1): 1–38.
7.         Baldursson S, Karanis P. Waterborne transmission of protozoan parasites: Review of worldwide outbreaks – an update 2004–2010. Water Res 2011; 45(20): 6603–14.
8.         Plutzer J, Karanis P, Domokos K, Törökné A, Márialigeti K. Detection and characterisation of Giardia and Cryptosporidium in Hungarian raw, surface and sewagewater samples by IFT, PCR and sequence analysis of the SSUrRNA and GDH genes. Int J Hyg Environ Health 2008; 211(5-6): 524–33.
9.         Mahmoudi MR, Kazemi B, Haghighi A, Karanis P. Detection of Acanthamoeba and Toxoplasma in river water samples by molecular methods in Iran. Iran J Parasitol 2015; 10(2): 250-7.
10.       Mahmoudi MR, Ashrafi K, Abedinzadeh H, Tahvildar-Bideruni F, Haghighi A, Bandehpour M, et al. Development of sensitive detection of Cryptosporidium and Giardia from surface water in iran. Iran J Parasitol 2011; 6(3): 43-51.
11.       Toledo RD, Martins FD, Ferreira FP, de Almeida JC, Ogawa L, Dos Santos HL, et al. Cryptosporidium spp. and Giardia spp. in feces and water and the associated exposure factors on dairy farms. PLoS One 2017; 12(4): e0175311.
12.       Matavos-Aramyan S, Moussavi M, Matavos-Aramyan H, Roozkhosh S. Cryptosporidium-contaminated water disinfection by a novel Fenton process. Free Radic Biol Med 2017; 106: 158-67.
13.       Gallas-Lindemann C, Sotiriadou I, Plutzer J, Noack MJ, Mahmoudi MR, Karanis P. Giardia and Cryptosporidium spp. dissemination during wastewater treatment and comparative detection via immunofluorescence assay (IFA), nested polymerase chain reaction (nested PCR) and loop mediated isothermal amplification (LAMP). Acta Trop 2016;158:43-51.
14. Bilung LM, Tahar AS, Yunos NE, Apun K, Lim YAL, Nillian E, et al. Detection of Cryptosporidium and Cyclospora oocysts from environmental water for drinking and recreational activities in Sarawak, Malaysia. BioMed Research International  2017; (3): 1-9
15.       Xiao L, Singh A, Limor J, Graczyk TK, Gradus S, Lal A. Molecular characterization of Cryptosporidium oocysts in samples of raw surface water and wastewater. Appl Environ Microbiol 2001; 67(3): 1097–101.
16.       Mahmoudi MR, Kazemi B, Mohammadiha A, Mirzaei A, Karanis P. Detection of Cryptosporidium and Giardia (oo)cysts by IFA, PCR and LAMP in surface water from Rasht, Iran. Trans R Soc Trop Med Hyg 2013;107(8):511-7.
17.       Mahmoudi MR, Nazemalhosseini-Mojarad E, Kazemi B, Haghighi A, Mirzaei A, Mohammadiha A, et al. Cryptosporidium genotypes and subtypes distribution in river water in Iran. J Water Health 2015;13(2):600-6..
18.       Manouchehri Naeini K, Asadi M, Hashemzade Chaleshtori M. Detection and molecular characterization of Cryptosporidium species in recreational waters of Chaharmahal va Bakhtiyari province of Iran using nested-PCR-RFLP. Iran J Parasitol 2001;6(1):20–7.
19.       Muchiri JM, Ascolillo L, Mugambi M, Mutwiri T, Ward HD, Naumova EN, et al. Seasonality of Cryptosporidium oocyst detection in surface waters of Meru, Kenya as determined by two isolation methods followed by PCR. J Water Health 2009; 7(1): 67-75.
20.       Castro-Hermida JA, García-Presedo I, Almeida A, González-Warleta M, Correia Da Costa JM, Mezo M. Contribution of treated wastewater to the contamination of recreational river areas with Cryptosporidium spp. and Giardia duodenalis. Water Res 2008; 42(13): 3528–38.
21.       Hänninen ML, Hörman A, Rimhanen-Finne R, Vahtera H, Malmberg S, Herve S, Lahti K. Monitoring of Cryptosporidium and Giardia in the Vantaa river basin, southern Finland. Int J Hyg Environ Health 2005; 208(3): 163–71.
22.       Xiao S, Yin P, Zhang Y, Hu S. Occurrence of Cryptosporidium and Giardia and the relationship between protozoa and water quality indicators in swimming pools. Korean J Parasitol 2017; 55(2): 129-35.
23.      Zahedi A, Monis P, Aucote S, King B, Paparini A, Jian F, et al. Zoonotic Cryptosporidium species in animals inhabiting Sydney water catchments. PLoS One 2016; 11(12): e0168169.
24.       Koloren Z, Ayaz E. Genotyping of Cryptosporidium spp. in environmental water in Turkey. Acta Parasitol 2016; 61(4): 671-9.
25.       Pirestani M, Sadraei J, Dalimi asl A, Zavvar M, Vaeznia H. Molecular characterization of Cryptosporidium isolates from human and bovine using 18 rRNA gene in Shahriar county of Tehran, Iran. Parasitol Res 2008;103(2):467–72.
26.       Zavvar M, Sadraei J, Emadi H, Pirestani M. The use of a nested PCR–RFLP technique, based on the parasite’s 18S ribosomal RNA, to characterize Cryptosporidium isolates from HIV/AIDS patients. Ann Trop Med Parasitol 2008;102(7):597–601.
27.       Daniels ME, Smith WA, Schmidt WP, Clasen T, Jenkins MW. Modeling Cryptosporidium and Giardia in ground and surface water sources in rural India: Associations with latrines, livestock, damaged wells, and rainfall patterns. Environ Sci Technol 2016; 50(14): 7498-507.
28.       Maciel PMF, Sabogal-Paz LP. Removal of Giardia spp. and Cryptosporidium spp. from water supply with high turbidity: Analytical challenges and perspectives. J Water Health 2016; 14(3): 369-78.
29.       Koehler AV, Haydon SR, Jex AR, Gasser RB. Cryptosporidium and Giardia taxa in faecal samples from animals in catchments supplying the city of Melbourne with drinking water (2011 to 2015). Parasit Vectors 2016; 9(1): 315.
30.       Chuah CJ, Mukhaidin N, Choy SH, Smith GJD, Mendenhall IH, Lim YAL, et al. Prevalence of Cryptosporidium and Giardia in the water resources of the Kuang River catchment, Northern Thailand. Sci Total Environ 2016; 562: 701-13.
31.       Sterk A, Schijven J, de Roda Husman AM, de Nijs T. Effect of climate change on runoff of Campylobacter and Cryptosporidium from land to surface water. Water Res 2016; 95: 90-102.
32.       Kumar T, Abd Majid MA, Onichandran S, Jaturas N, Andiappan H, Salibay CC, et al. Presence of Cryptosporidium parvum and Giardia lamblia in water samples from Southeast Asia: Towards an integrated water detection system. Infect Dis Poverty 2016; 5: 3.
33.       Headd B, Bradford SA. Use of aerobic spores as a surrogate for Cryptosporidium oocysts in drinking water supplies. Water Res 2016; 90: 185-202.
34.       Hawash Y, Ghonaim M, Hussein Y, Alhazmi A, Alturkistani A. Identification of Giardia lamblia and the human infectious-species of Cryptosporidium in drinking water resources in Western Saudi Arabia by nested-PCR assays. Trop Biomed 2015; 32(2): 216-24.
35.       Zahedi A, Paparini A, Jian F, Robertson I, Ryan U. Public health significance of zoonotic Cryptosporidium species in wildlife: Critical insights into better drinking water management. Int J Parasitol Parasites Wildl 2016; 5(1): 88-109.
36.       Mesdaghinia A, Younesian M, Nasseri S, Nabizadeh Nodehi R, Hadi M. A bibliometric and trend analysis on the water-related risk assessment studies for Cryptosporidium pathogen. Iran J Parasitol 2015; 10(3): 338-50.
37.       Murphy HM, Thomas MK, Schmidt PJ, Medeiros DT, McFadyen S, Pintar KDM. Estimating the burden of acute gastrointestinal illness due to Giardia, Cryptosporidium, Campylobacter, E. coli O157 and norovirus associated with private wells and small water systems in Canada. Epidemiol Infect 2016; 144(7): 1355-70.
38.       Abeledo-Lameiro MJ, Ares-Mazas E, Gomez-Couso H. Evaluation of solar photocatalysis using TiO2 slurry in the inactivation of Cryptosporidium parvum oocysts in water. J Photochem Photobiol B 2016; 163: 92-9.
39. Xiao L, Cama VA, Cabrera L, Ortega Y, Pearson J, Gilman RH. Possible transmission of Cryptosporidium canis among children and a dog in a household. J Clin Microbiol 2007; 45(6): 2014–6.