Seroprevalence of Cryptosporidium and risks of cryptosporidiosis in residents of Sothern Egypt: A cross-sectional study
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摘要
Objective: To identify the serological epidemiology of Cryptosporidium infections and to follow up on the changes in the infection profile in Southern Egypt in order to establish a suitable scheme for control and prevention of cryptosporidiosis.Methods: A total of 1 912(960 from human and 952 from animals) stool specimens and sera were screened for Cryptosporidium species using modified Ziehl Neelsen technique and a newly-developed enzyme-linked immunosorbent assay(ELISA).Environmental risk factors and socioeconomic data were surveyed by questionnaire between September 2016 and December 2017.Results: Totally, 20.83% of the human subjects were positive for Cryptosporidium infection tested by ELISA.The seropositivity was positively correlated with age.The prevalence of Cryptosporidium infections in females was significantly higher than in males(P<0.05).The sensitivity and specificity of ELISA for Cryptosporidium were 99.06% and 88.88%, respectively.Furthermore, a high prevalence of Cryptosporidium in domestic animals(42.20%).Conclusions: The study observed that Cryptosporidium infections are common in the study area, with water sanitation, socioeconomic level; eating habits and hygienic status are considered the main risk factors for cryptosporidiosis.Therefore, environmental sanitation and health education will be useful in reducing the prevalence of infection.
Objective: To identify the serological epidemiology of Cryptosporidium infections and to follow up on the changes in the infection profile in Southern Egypt in order to establish a suitable scheme for control and prevention of cryptosporidiosis.Methods: A total of 1 912(960 from human and 952 from animals) stool specimens and sera were screened for Cryptosporidium species using modified Ziehl Neelsen technique and a newly-developed enzyme-linked immunosorbent assay(ELISA).Environmental risk factors and socioeconomic data were surveyed by questionnaire between September 2016 and December 2017.Results: Totally, 20.83% of the human subjects were positive for Cryptosporidium infection tested by ELISA.The seropositivity was positively correlated with age.The prevalence of Cryptosporidium infections in females was significantly higher than in males(P<0.05).The sensitivity and specificity of ELISA for Cryptosporidium were 99.06% and 88.88%, respectively.Furthermore, a high prevalence of Cryptosporidium in domestic animals(42.20%).Conclusions: The study observed that Cryptosporidium infections are common in the study area, with water sanitation, socioeconomic level; eating habits and hygienic status are considered the main risk factors for cryptosporidiosis.Therefore, environmental sanitation and health education will be useful in reducing the prevalence of infection.
Objective: To identify the serological epidemiology of Cryptosporidium infections and to follow up on the changes in the infection profile in Southern Egypt in order to establish a suitable scheme for control and prevention of cryptosporidiosis.Methods: A total of 1 912(960 from human and 952 from animals) stool specimens and sera were screened for Cryptosporidium species using modified Ziehl Neelsen technique and a newly-developed enzyme-linked immunosorbent assay(ELISA).Environmental risk factors and socioeconomic data were surveyed by questionnaire between September 2016 and December 2017.Results: Totally, 20.83% of the human subjects were positive for Cryptosporidium infection tested by ELISA.The seropositivity was positively correlated with age.The prevalence of Cryptosporidium infections in females was significantly higher than in males(P<0.05).The sensitivity and specificity of ELISA for Cryptosporidium were 99.06% and 88.88%, respectively.Furthermore, a high prevalence of Cryptosporidium in domestic animals(42.20%).Conclusions: The study observed that Cryptosporidium infections are common in the study area, with water sanitation, socioeconomic level; eating habits and hygienic status are considered the main risk factors for cryptosporidiosis.Therefore, environmental sanitation and health education will be useful in reducing the prevalence of infection.
引文
[1]Laude A,Valot S,Desoubeaux G,Argy N,Nourrisson C,Pomares C,et al.Is real-time PCR-based diagnosis similar in performance to routine parasitological examination for the identification of Giardia intestinalis,Cryptosporidium parvum/Cryptosporidium hominis and Entamoeba histolytica from stool samples?Evaluation of a new commercial multiplex PCR assay and literature review.Clin Microbiol Infect 2016;22:190.
[2]Xiao L,Ryan UM.Cryptosporidiosis:An update in molecular epidemiology.Curr Opin Infect Dis 2004;17:483-490.
[3]Agnamey P,Sarfati C,Pinel C,Rabodoniriina M,Kapel N,Dutoit E,et al.Evaluation of four commercial rapid immunochromatographic assays for detection of Cryptosporidium antigens in stool samples:A blind multicenter trial.J Clin Microbiol 2011;49:1605-1607.
[4]Putignani L,Menichella D.Global distribution,public health and clinical impact of the protozoan pathogen Cryptosporidium.Interdiscip Perspect Infect Dis 2010;2010:1-39.
[5]Bouzid M,Kintz E,Hunter PR.Risk factors for Cryptosporidium infection in low-and middle-income countries:A systematic review and metaanalysis.PLo S Negl Trop Dis 2018;12(6):e0006553.
[6]Sarkar R,Ajjampur SSR,Prabakaran AD,Geetha JC,Sowmyanarayanan TV,Kane A,et al.Cryptosporidiosis among children in an endemic semiurban community in Southern India:Does a protected drinking water source decrease infection?Clin Infect Dis 2013;57(3):398-406.
[7]Amer S,Honma H,Ikarashi M,Tada C,Fukuda Y,Suyama Y,et al.Cryptosporidium genotypes and subtypes in dairy calves in Egypt.Vet Parasitol 2010;169(3-4):382-386.
[8]Youssef FG,Adib I,Riddle MS,Schlett CD.A review of cryptosporidiosis in Egypt.J Egypt Soc Parasitol 2008;38(1):9-28.
[9]Datt,G,Jolliffe D.Poverty in Egypt:Modeling and policy simulations.Econ Develop Cult Change 2005;53(2):327-346.
[10]Dryden MW,Payne PA,Ridley R,Smith V.Comparison of common fecal flotation techniques for the recovery of parasite eggs and oocysts.Vet Ther 2005;6(1):15-28.
[11]Tahvildar-Biderouni F,Salehi N.Detection of Cryptosporidium infection by modified Ziehl-Neelsen and PCR methods in children with diarrheal samples in pediatric hospitals in Tehran.Gastroenterol Hepatol Bed Bench2014;7(2):125-130
[12]Loong TW.Understanding sensitivity and specificity with the right side of the brain.BMJ 2003;7327(7417):716-719.
[13]Derouin F,Dutoit E,de Monbrison F.ANOFEL Cryptosporidium National Network.Laboratory-based surveillance for Cryptosporidium in France,2006-2009.Euro Surveill 2010;15(33):19642.
[14]Abd El Kader NM,Blanco MA,Ali-Tammam M,Abd El Ghaffar R,Osman A.Detection of Cryptosporidium parvum and Cryptosporidium hominis in human patients in Cairo,Egypt.Parasitol Res 2012;110:161-166.
[15]Shoukry NM,Dawoud HA,Haridy FM.Studies on zoonotic cryptosporidiosis parvum in Ismailia Governorate,Egypt.J Egypt Soc Parasitol 2009;39:479-488.
[16]Allam AF,Shehab AY.Efficacy of azithromycin,praziquantel and mirazid in treatment of cryptosporidiosis in school children.J Egypt Soc Parasitol 2002;32:969-978.
[17]Munoz-Antoli C,Pavón A,Marcilla A,Toledo R,Esteban JG.Prevalence and molecular characterization of Cryptosporidium in school children from department of Rio San Juan(Nicaragua).Trop Biomed 2011;28(1):40-47.
[18]Yoder JS,Beach MJ.Cryptosporidium surveillance and risk factors in the United States.Exp Parasitol 2010;124(1):31-39.
[19]Bezerra FSM,Troiani RM,Parente TML,Paiva ARA,Queiroz RMP,Coelho JR,et al.Incidence of cryptosporidise in children with moderate to severe internal malnutrition in the IPREDE(Institute for the Prevention of malnutrition and exceptionality)in Fortaleza-CE.Rev Soc Bras Med Trop 2001;34:300.
[20]Yu JR,Lee JK,Seo M,Kim SI,Sohn WM,Huh S,et al.Prevalence of cryptosporidiosis among the villagers and domestic animals in several rural areas of Korea.Korean J Parasitol 2004;42:1-6.
[21]Kosek M,Alcantara C,Lima AA,Guerrant RL.Cryptosporidiosis:An update.Lancet Infect Dis 2001;1:262-269.
[22]Laubach HE,Bentley CZ,Ginter EL,Spalter J,Jensen LA.A study of risk factors associated with the prevalence of Cryptosporidium in villages around Lake Atitlan,Guatemala.Braz J Infect Dis 2004;8(4):319-323.
[23]Egberongbe HO,Agbolade OM,Adesetan TO,Olufemi M,Titilayo AO,Oladele MO,et al.Cryptosporidiosis among children in relation to toilet facilities and water sources in Ijebu and Remo areas,southwestern Nigeria.J Med Sci 2010;1(10):485-489.
[24]Saneian H,Yaghini O,Yaghini A,Modarresi MR,Soroshnia M.Infection rate of Cryptosporidium parvum among diarrhoeic children in Isfahan.Iran J Pediatr 2010;20(3):343-347.
[25]Fuchslin HP,Kotzch S,Egli T.Cryptosporidium spp.in drinking water.Samples from rural sites in Switzerland.Swiss Med Wkly 2012;142:w13683.doi:10.4414/smw.2012.13683.
[26]Castro-Hermida JA,Garcia-Presedo I,Almeida A,González-Warleta M,Correia Da Costa JM,Mezo M.Presence of Cryptosporidium spp.and Giardia duodenalis through drinking water.Sci Total Environ 2008;405:45-53.
[27]Mons C,Dumetre A,Gosselin S,Galliot C,Moulin L.Monitoring of Cryptosporidium and Giardia river contamination in Paris area.Water Res2009;43:211-217.
[28]Lake IR,Nichols G,Harrison FD,Bentham G,Sari Kovats R,Grundy C,et al.Using infectious intestinal disease surveillance data to explore illness aetiology:A cryptosporidiosis case study.Health Place 2009;15:333-339.
[29]Nichols G.Epidemiology.In:Fayer R,Xiao L,editors.Cryptosporidium and cryptosporidiosis.2nd edition.Taylors&Francis Group:USA;2008,p.79-118.
[30]Ryan UM.Cryptosporidium in birds,fish and amphibians.Exp Parasitol2010;124:113-120.
[31]Carvalho TB,Carvalho LR,Mascarini LM.Occurrence of enteroparasites in day care centers in Botucatu(S?ao Paulo State,Brazil)with emphasis on Cryptosporidium sp.,Giardia duodenalis and Enterobius vermicularis.Rev Inst Med Trop Sao Paulo 2006;48(5):269-273.
[32]Amin OM.Seasonal prevalence of intestinal parasites in the United States during 2000.Am J Trop Med Hyg 2002;66:799-803.
[33]Philippa MB,Robinson G,Elwin K,Tyler K,Hunter P,Chalmers R.Prevalence and epidemiology of human Cryptosporidium parvum IIc infections in England and Wales.Lancet 2017;389(1):S1.
[34]Iqbal J,Hira PR,Al-Ali F,Philip R.Cryptosporidiosis in Kuwaiti children:Seasonality and endemicity.Clin Microbiol Infect 2001;7(5):261-266.
[35]Chalmers RM,Davies AP.Minireview:Clinical cryptosporidiosis.Exp Parasitol 2010;124(1):138-146.
[36]Thabet FS,El-Shahawy GA,Shalaby MA,Sabry HY,Matooq PM,Elmallah AM.Detection rates of waterborne protozoa in water sources from Fayoum Governorate.Parasitol Unit J 2017;10(1-2):30-38.
[37]Hassl A,Benyr G,Sommer R.Occurrence of Cryptosporidium sp.oocysts in Fecal and water samples in Austria.Acta Trop 2001;80:145-149.
[38]Antonios SN,Salem SA,Khalifa EA.Water pollution is a risk factor for Cryptosporidium infection in Gharbia Governorate.J Egypt Soc Parasitol2001;31(3):963-964.
[39]Betancourt WQ,Rose JB.Drinking water treatment processes for removal of Cryptosporidium and Giardia.Vet Parasitol 2004;126:219-234.
[40]\Ramirez NE,Ward LA,Sreevatsan S.A review of the biology and epidemiology of cryptosporidiosis in humans and animals.Microbes Infect 2004;6(8):773-785.
[41]Tariuwa HO,Ajogi I,Ejembi CL,Awah IJ,Green PA,Fadipe EO,et al.Incidence of Cryptosporidium infection in port-harcourt rivers state Nigeria based on regular contact with domestic animals.Nigerian Vet J2007;28(3):1-5.
[42]Zambrano LD,Levy K,Menezes N,Freeman MC.Human diarrhea infections associated with domestic animal husbandry:A systematic review and meta-analysis.Trans R Soc Trop Med Hyg 2014;108(6):313-325.
[43]Mahfouz ME,Mira N,Amer S.Prevalence and Genotyping of Cryptosporidium spp.in farm animals in Egypt.J Vet Med Sci 2014;76(12):1569-1575.
[44]Sazmand A,Rasooli A,Nouri M,Hamidinejat H,Hekmatimoghaddam S.Prevalence of Cryptosporidium spp.in camels and involved people in Yazd Province,Iran.Iran J Parasitol 2012;7(1):80-84.
[45]Zaglool D,Mohamed A,Khodari Y,Farooq MU.Crypto-Giardia antigen rapid test versus conventional modified Ziehl-Neelsen acid fast staining method for diagnosis of cryptosporidiosis.Asian Pac J Trop Med 2013;5:212-215.
[2]Xiao L,Ryan UM.Cryptosporidiosis:An update in molecular epidemiology.Curr Opin Infect Dis 2004;17:483-490.
[3]Agnamey P,Sarfati C,Pinel C,Rabodoniriina M,Kapel N,Dutoit E,et al.Evaluation of four commercial rapid immunochromatographic assays for detection of Cryptosporidium antigens in stool samples:A blind multicenter trial.J Clin Microbiol 2011;49:1605-1607.
[4]Putignani L,Menichella D.Global distribution,public health and clinical impact of the protozoan pathogen Cryptosporidium.Interdiscip Perspect Infect Dis 2010;2010:1-39.
[5]Bouzid M,Kintz E,Hunter PR.Risk factors for Cryptosporidium infection in low-and middle-income countries:A systematic review and metaanalysis.PLo S Negl Trop Dis 2018;12(6):e0006553.
[6]Sarkar R,Ajjampur SSR,Prabakaran AD,Geetha JC,Sowmyanarayanan TV,Kane A,et al.Cryptosporidiosis among children in an endemic semiurban community in Southern India:Does a protected drinking water source decrease infection?Clin Infect Dis 2013;57(3):398-406.
[7]Amer S,Honma H,Ikarashi M,Tada C,Fukuda Y,Suyama Y,et al.Cryptosporidium genotypes and subtypes in dairy calves in Egypt.Vet Parasitol 2010;169(3-4):382-386.
[8]Youssef FG,Adib I,Riddle MS,Schlett CD.A review of cryptosporidiosis in Egypt.J Egypt Soc Parasitol 2008;38(1):9-28.
[9]Datt,G,Jolliffe D.Poverty in Egypt:Modeling and policy simulations.Econ Develop Cult Change 2005;53(2):327-346.
[10]Dryden MW,Payne PA,Ridley R,Smith V.Comparison of common fecal flotation techniques for the recovery of parasite eggs and oocysts.Vet Ther 2005;6(1):15-28.
[11]Tahvildar-Biderouni F,Salehi N.Detection of Cryptosporidium infection by modified Ziehl-Neelsen and PCR methods in children with diarrheal samples in pediatric hospitals in Tehran.Gastroenterol Hepatol Bed Bench2014;7(2):125-130
[12]Loong TW.Understanding sensitivity and specificity with the right side of the brain.BMJ 2003;7327(7417):716-719.
[13]Derouin F,Dutoit E,de Monbrison F.ANOFEL Cryptosporidium National Network.Laboratory-based surveillance for Cryptosporidium in France,2006-2009.Euro Surveill 2010;15(33):19642.
[14]Abd El Kader NM,Blanco MA,Ali-Tammam M,Abd El Ghaffar R,Osman A.Detection of Cryptosporidium parvum and Cryptosporidium hominis in human patients in Cairo,Egypt.Parasitol Res 2012;110:161-166.
[15]Shoukry NM,Dawoud HA,Haridy FM.Studies on zoonotic cryptosporidiosis parvum in Ismailia Governorate,Egypt.J Egypt Soc Parasitol 2009;39:479-488.
[16]Allam AF,Shehab AY.Efficacy of azithromycin,praziquantel and mirazid in treatment of cryptosporidiosis in school children.J Egypt Soc Parasitol 2002;32:969-978.
[17]Munoz-Antoli C,Pavón A,Marcilla A,Toledo R,Esteban JG.Prevalence and molecular characterization of Cryptosporidium in school children from department of Rio San Juan(Nicaragua).Trop Biomed 2011;28(1):40-47.
[18]Yoder JS,Beach MJ.Cryptosporidium surveillance and risk factors in the United States.Exp Parasitol 2010;124(1):31-39.
[19]Bezerra FSM,Troiani RM,Parente TML,Paiva ARA,Queiroz RMP,Coelho JR,et al.Incidence of cryptosporidise in children with moderate to severe internal malnutrition in the IPREDE(Institute for the Prevention of malnutrition and exceptionality)in Fortaleza-CE.Rev Soc Bras Med Trop 2001;34:300.
[20]Yu JR,Lee JK,Seo M,Kim SI,Sohn WM,Huh S,et al.Prevalence of cryptosporidiosis among the villagers and domestic animals in several rural areas of Korea.Korean J Parasitol 2004;42:1-6.
[21]Kosek M,Alcantara C,Lima AA,Guerrant RL.Cryptosporidiosis:An update.Lancet Infect Dis 2001;1:262-269.
[22]Laubach HE,Bentley CZ,Ginter EL,Spalter J,Jensen LA.A study of risk factors associated with the prevalence of Cryptosporidium in villages around Lake Atitlan,Guatemala.Braz J Infect Dis 2004;8(4):319-323.
[23]Egberongbe HO,Agbolade OM,Adesetan TO,Olufemi M,Titilayo AO,Oladele MO,et al.Cryptosporidiosis among children in relation to toilet facilities and water sources in Ijebu and Remo areas,southwestern Nigeria.J Med Sci 2010;1(10):485-489.
[24]Saneian H,Yaghini O,Yaghini A,Modarresi MR,Soroshnia M.Infection rate of Cryptosporidium parvum among diarrhoeic children in Isfahan.Iran J Pediatr 2010;20(3):343-347.
[25]Fuchslin HP,Kotzch S,Egli T.Cryptosporidium spp.in drinking water.Samples from rural sites in Switzerland.Swiss Med Wkly 2012;142:w13683.doi:10.4414/smw.2012.13683.
[26]Castro-Hermida JA,Garcia-Presedo I,Almeida A,González-Warleta M,Correia Da Costa JM,Mezo M.Presence of Cryptosporidium spp.and Giardia duodenalis through drinking water.Sci Total Environ 2008;405:45-53.
[27]Mons C,Dumetre A,Gosselin S,Galliot C,Moulin L.Monitoring of Cryptosporidium and Giardia river contamination in Paris area.Water Res2009;43:211-217.
[28]Lake IR,Nichols G,Harrison FD,Bentham G,Sari Kovats R,Grundy C,et al.Using infectious intestinal disease surveillance data to explore illness aetiology:A cryptosporidiosis case study.Health Place 2009;15:333-339.
[29]Nichols G.Epidemiology.In:Fayer R,Xiao L,editors.Cryptosporidium and cryptosporidiosis.2nd edition.Taylors&Francis Group:USA;2008,p.79-118.
[30]Ryan UM.Cryptosporidium in birds,fish and amphibians.Exp Parasitol2010;124:113-120.
[31]Carvalho TB,Carvalho LR,Mascarini LM.Occurrence of enteroparasites in day care centers in Botucatu(S?ao Paulo State,Brazil)with emphasis on Cryptosporidium sp.,Giardia duodenalis and Enterobius vermicularis.Rev Inst Med Trop Sao Paulo 2006;48(5):269-273.
[32]Amin OM.Seasonal prevalence of intestinal parasites in the United States during 2000.Am J Trop Med Hyg 2002;66:799-803.
[33]Philippa MB,Robinson G,Elwin K,Tyler K,Hunter P,Chalmers R.Prevalence and epidemiology of human Cryptosporidium parvum IIc infections in England and Wales.Lancet 2017;389(1):S1.
[34]Iqbal J,Hira PR,Al-Ali F,Philip R.Cryptosporidiosis in Kuwaiti children:Seasonality and endemicity.Clin Microbiol Infect 2001;7(5):261-266.
[35]Chalmers RM,Davies AP.Minireview:Clinical cryptosporidiosis.Exp Parasitol 2010;124(1):138-146.
[36]Thabet FS,El-Shahawy GA,Shalaby MA,Sabry HY,Matooq PM,Elmallah AM.Detection rates of waterborne protozoa in water sources from Fayoum Governorate.Parasitol Unit J 2017;10(1-2):30-38.
[37]Hassl A,Benyr G,Sommer R.Occurrence of Cryptosporidium sp.oocysts in Fecal and water samples in Austria.Acta Trop 2001;80:145-149.
[38]Antonios SN,Salem SA,Khalifa EA.Water pollution is a risk factor for Cryptosporidium infection in Gharbia Governorate.J Egypt Soc Parasitol2001;31(3):963-964.
[39]Betancourt WQ,Rose JB.Drinking water treatment processes for removal of Cryptosporidium and Giardia.Vet Parasitol 2004;126:219-234.
[40]\Ramirez NE,Ward LA,Sreevatsan S.A review of the biology and epidemiology of cryptosporidiosis in humans and animals.Microbes Infect 2004;6(8):773-785.
[41]Tariuwa HO,Ajogi I,Ejembi CL,Awah IJ,Green PA,Fadipe EO,et al.Incidence of Cryptosporidium infection in port-harcourt rivers state Nigeria based on regular contact with domestic animals.Nigerian Vet J2007;28(3):1-5.
[42]Zambrano LD,Levy K,Menezes N,Freeman MC.Human diarrhea infections associated with domestic animal husbandry:A systematic review and meta-analysis.Trans R Soc Trop Med Hyg 2014;108(6):313-325.
[43]Mahfouz ME,Mira N,Amer S.Prevalence and Genotyping of Cryptosporidium spp.in farm animals in Egypt.J Vet Med Sci 2014;76(12):1569-1575.
[44]Sazmand A,Rasooli A,Nouri M,Hamidinejat H,Hekmatimoghaddam S.Prevalence of Cryptosporidium spp.in camels and involved people in Yazd Province,Iran.Iran J Parasitol 2012;7(1):80-84.
[45]Zaglool D,Mohamed A,Khodari Y,Farooq MU.Crypto-Giardia antigen rapid test versus conventional modified Ziehl-Neelsen acid fast staining method for diagnosis of cryptosporidiosis.Asian Pac J Trop Med 2013;5:212-215.