|
|
Cyclospora cayetanensis infections among diarrheal outpatients in Shanghai: a retrospective case study |
Yanyan Jiang1, Zhongying Yuan1, Guoqing Zang2, Dan Li2, Ying Wang1, Yi Zhang2, Hua Liu1, Jianping Cao1(), Yujuan Shen1() |
1. National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention; Key Laboratory of Parasite and Vector Biology, Ministry of Health, China; WHO Collaborating Center for Tropical Diseases, Shanghai 200025, China 2. Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, Shanghai 200233, China |
|
|
Abstract Cyclospora cayetanensis is a foodborne and waterborne pathogen that causes endemic and epidemic human diarrhea worldwide. A few epidemiological studies regarding C. cayetanensis infections in China have been conducted. During 2013, a total of 291 stool specimens were collected from patients with diarrhea at a hospital in urban Shanghai. C. cayetanensis was not detected in any of the stool specimens by traditional microscopy, whereas five stool specimens (1.72%, 5/291) were positive by PCR. These positive cases confirmed by molecular technology were all in the adult group (mean age 27.8 years; 2.94%, 5/170) with watery diarrhea. Marked infection occurred in the rainy season of May and July. Sequence and phylogenetic analyses of the partial 18S rRNA genes of C. cayetanensis isolated showed intra-species diversity of this parasite. This study showed, for the first time, that C. cayetanensis is a pathogen in outpatients with diarrhea in Shanghai, albeit at a low level. However, the transmission dynamics of this parasite in these patients remain uncertain.
|
Keywords
Cyclospora cayetanensis
outpatients with diarrhea
stool specimens
18S rRNA gene
|
Corresponding Author(s):
Jianping Cao,Yujuan Shen
|
Just Accepted Date: 03 January 2018
Online First Date: 26 January 2018
Issue Date: 06 February 2018
|
|
1 |
Thima K, Mori H, Praevanit R, Mongkhonmu S, Waikagul J, Watthanakulpanich D. Recovery of Cyclospora cayetanensis among asymptomatic rural Thai schoolchildren. Asian Pac J Trop Med 2014; 7(2): 119–123
https://doi.org/10.1016/S1995-7645(14)60006-7
pmid: 24461524
|
2 |
Llanes R, Velázquez B, Reyes Z, Somarriba L. Co-infection with Cyclospora cayetanensis and Salmonella typhi in a patient with HIV infection and chronic diarrhoea. Pathog Glob Health 2013; 107(1): 38–39
https://doi.org/10.1179/2047773212Y.0000000065
pmid: 23432863
|
3 |
Centers for Disease Control and Prevention (CDC). Outbreaks of cyclosporiasis—United States, June−August 2013. MMWR Morb Mortal Wkly Rep 2013; 62(43): 862
pmid: 24172881
|
4 |
Sánchez-Vega JT, Cabrera-Fuentes HA, Romero-Olmedo AJ, Ortiz-Frías JL, Sokolina F, Barreto G. Cyclospora cayetanensis: this emerging protozoan pathogen in Mexico. Am J Trop Med Hyg 2014; 90(2): 351–353
https://doi.org/10.4269/ajtmh.12-0782
pmid: 24379243
|
5 |
Chacín-Bonilla L, Estévez J, Monsalve F, Quijada L.Cyclospora cayetanensis infections among diarrheal patients from Venezuela. Am J Trop Med Hyg 2001; 65(4): 351–354
https://doi.org/10.4269/ajtmh.2001.65.351
pmid: 11693883
|
6 |
Milord F, Lampron-Goulet E, St-Amour M, Levac E, Ramsay D. Cyclospora cayetanensis: a description of clinical aspects of an outbreak in Quebec, Canada. Epidemiol Infect 2012; 140(4): 626–632
https://doi.org/10.1017/S095026881100121X
pmid: 21791150
|
7 |
Koru O, Araz E, Inci A, Tanyuksel M. Co-infection of Giardia intestinalis and Cyclospora cayetanensis in an immunocompetent patient with prolonged diarrhea: case report. J Microbiol 2006; 44(3): 360–362
pmid: 16820767
|
8 |
Chacín-Bonilla L. Transmission of Cyclospora cayetanensis infection: a review focusing on soil-borne cyclosporiasis. Trans R Soc Trop Med Hyg 2008; 102(3): 215–216
https://doi.org/10.1016/j.trstmh.2007.06.005
pmid: 17689579
|
9 |
Galván AL, Magnet A, Izquierdo F, Fenoy S, Rueda C, Fernández Vadillo C, Henriques-Gil N, del Aguila C. Molecular characterization of human-pathogenic microsporidia and Cyclospora cayetanensis isolated from various water sources in Spain: a year-long longitudinal study. Appl Environ Microbiol 2013; 79(2): 449–459
https://doi.org/10.1128/AEM.02737-12
pmid: 23124243
|
10 |
Ben Ayed L, Yang W, Widmer G, Cama V, Ortega Y, Xiao L. Survey and genetic characterization of wastewater in Tunisia for Cryptosporidium spp., Giardia duodenalis, Enterocytozoon bieneusi, Cyclospora cayetanensis and Eimeria spp. J Water Health 2012; 10(3): 431–444
https://doi.org/10.2166/wh.2012.204
pmid: 22960487
|
11 |
Chacín-Bonilla L, Barrios F, Sanchez Y. Epidemiology of Cyclospora cayetanensis infection in San Carlos Island, Venezuela: strong association between socio-economic status and infection. Trans R Soc Trop Med Hyg 2007; 101(10): 1018–1024
https://doi.org/10.1016/j.trstmh.2007.05.008
pmid: 17655898
|
12 |
Xing WL, Wu KW, Ling XY, Huang HC, Liu QZ, Zheng XY, Jin YG. Prevalence survey on Cyclospora cayetanensis in diarrhea cases in Wenzhou. Chin J Parasit Dis Control (Zhongguo Ji Sheng Chong Bing Fang Zhi Za Zhi) 2002; 15(5): 320–321 (in Chinese)
|
13 |
Wang KX, Li CP, Wang J, Tian Y. Cyclospore cayetanensis in Anhui, China. World J Gastroenterol 2002; 8(6): 1144–1148
https://doi.org/10.3748/wjg.v8.i6.1144
pmid: 12439942
|
14 |
Zhang BX, Yu H, Zhang LL, Tao H, Li YZ, Li Y, Cao ZK, Bai ZM, He YQ. Prevalence survey on Cyclospora cayetanensis and Cryptosporidium ssp. in diarrhea cases in Yunnan Province. Chin J Parasitol Parasit Dis (Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi) 2002; 20(2): 106–108 (in Chinese)
pmid: 12567573
|
15 |
Berlin OG, Peter JB, Gagne C, Conteas CN, Ash LR. Autofluorescence and the detection of Cyclospora oocysts. Emerg Infect Dis 1998; 4(1): 127–128
https://doi.org/10.3201/eid0401.980121
pmid: 9452408
|
16 |
Swarna SR, Madhavan R, Gomathi S, Yadav D. Chronic diarrhea due to Cyclospora spp. infection. Trop Parasitol 2013; 3(1): 85–86
https://doi.org/10.4103/2229-5070.113924
pmid: 23961450
|
17 |
Sulaiman IM, Ortega Y, Simpson S, Kerdahi K. Genetic characterization of human-pathogenic Cyclospora cayetanensis parasites from three endemic regions at the 18S ribosomal RNA locus. Infect Genet Evol 2014; 22: 229–234
https://doi.org/10.1016/j.meegid.2013.07.015
pmid: 23891667
|
18 |
Kimura K, Rai SK, Rai G, Insisiengmay S, Kawabata M, Karanis P, Uga S. Study on Cyclospora cayetanensis associated with diarrheal disease in Nepal and Loa PDR. Southeast Asian J Trop Med Public Health 2005; 36(6): 1371–1376
pmid: 16610636
|
19 |
Gonçalves EM, Uemura IH, Castilho VL, Corbett CE. Retrospective study of the occurrence of Cyclospora cayetanensis at Clinical Hospital of the University of São Paulo Medical School, SP. Rev Soc Bras Med Trop 2005; 38(4): 326–330
https://doi.org/10.1590/S0037-86822005000400009
pmid: 16082480
|
20 |
Orozco-Mosqueda GE, Martínez-Loya OA, Ortega YR. Cyclospora cayetanensis in a pediatric hospital in Morelia, México. Am J Trop Med Hyg 2014; 91(3): 537–540
https://doi.org/10.4269/ajtmh.13-0535
pmid: 24957545
|
21 |
Hussein EM, El-Moamly AA, Mahmoud MA, Ateek NS. Wide genetic variations at 18S ribosomal RNA locus of Cyclospora cayetanensis isolated from Egyptian patients using high resolution melting curve. Parasitol Res 2016; 115(7): 2797–2806
https://doi.org/10.1007/s00436-016-5029-y
pmid: 27041342
|
22 |
Bern C, Kawai V, Vargas D, Rabke-Verani J, Williamson J, Chavez-Valdez R, Xiao L, Sulaiman I, Vivar A, Ticona E, Navincopa M, Cama V, Moura H, Secor WE, Visvesvara G, Gilman RH. The epidemiology of intestinal microsporidiosis in patients with HIV/AIDS in Lima, Peru. J Infect Dis 2005; 191(10): 1658–1664
https://doi.org/10.1086/429674
pmid: 15838792
|
23 |
Madico G, McDonald J, Gilman RH, Cabrera L, Sterling CR. Epidemiology and treatment of Cyclospora cayetanensis infection in Peruvian children. Clin Infect Dis 1997; 24(5): 977–981
https://doi.org/10.1093/clinids/24.5.977
pmid: 9142805
|
24 |
Pieniazek NJ, Slemenda SB, da Silva AJ, Alfano EM, Arrowood MJ. PCR confirmation of infection with Cyclospora cayetanensis. Emerg Infect Dis 1996; 2(4): 357–359
https://doi.org/10.3201/eid0204.960415
pmid: 8969255
|
25 |
Zhou Y, Lv B, Wang Q, Wang R, Jian F, Zhang L, Ning C, Fu K, Wang Y, Qi M, Yao H, Zhao J, Zhang X, Sun Y, Shi K, Arrowood MJ, Xiao L. Prevalence and molecular characterization of Cyclospora cayetanensis, Henan, China. Emerg Infect Dis 2011; 17(10): 1887–1890
https://doi.org/10.3201/eid1710.101296
pmid: 22000362
|
26 |
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28(10): 2731–2739
https://doi.org/10.1093/molbev/msr121
pmid: 21546353
|
27 |
Liu H, Shen Y, Yin J, Yuan Z, Jiang Y, Xu Y, Pan W, Hu Y, Cao J. Prevalence and genetic characterization of Cryptosporidium, Enterocytozoon, Giardia and Cyclospora in diarrheal outpatients in China. BMC Infect Dis 2014; 14(1): 25
https://doi.org/10.1186/1471-2334-14-25
pmid: 24410985
|
28 |
Eberhard ML, da Silva AJ, Lilley BG, Pieniazek NJ. Morphologic and molecular characterization of new Cyclospora species from Ethiopian monkeys: C. cercopitheci sp.n., C. colobi sp.n., and C. papionis sp.n. Emerg Infect Dis 1999; 5(5): 651–658
https://doi.org/10.3201/eid0505.990505
pmid: 10511521
|
29 |
Kaminsky RGLJ, Lagos J, Raudales Santos G, Urrutia S. Marked seasonality of Cyclospora cayetanensis infections: ten-year observation of hospital cases, Honduras. BMC Infect Dis 2016; 16(1): 66
https://doi.org/10.1186/s12879-016-1393-6
pmid: 26847438
|
30 |
Bern C, Arrowood MJ, Eberhard M, Maguire JH, Pratdesaba R, Torres O, Gonzalez M. Cyclospora in Guatemala: further considerations. J Clin Microbiol 2002; 40(2): 731–732
https://doi.org/10.1128/JCM.40.2.731-732.2002
pmid: 11826011
|
31 |
Bern C, Hernandez B, Lopez MB, Arrowood MJ, de Mejia MA, de Merida AM, Hightower AW, Venczel L, Herwaldt BL, Klein RE. Epidemiologic studies of Cyclospora cayetanensis in Guatemala. Emerg Infect Dis 1999; 5(6): 766–774
https://doi.org/10.3201/eid0506.990604
pmid: 10603209
|
32 |
Alakpa GE, Clarke SC, Fagbenro-Beyioku AF. Cyclospora cayetanensis infection in Lagos, Nigeria. Clin Microbiol Infect 2003; 9(7): 731–733
https://doi.org/10.1046/j.1469-0691.2003.00583.x
pmid: 12925119
|
33 |
Lopez AS, Bendik JM, Alliance JY, Roberts JM, da Silva AJ, Moura IN, Arrowood MJ, Eberhard ML, Herwaldt BL. Epidemiology of Cyclospora cayetanensis and other intestinal parasites in a community in Haiti. J Clin Microbiol 2003; 41(5): 2047–2054
https://doi.org/10.1128/JCM.41.5.2047-2054.2003
pmid: 12734247
|
34 |
Abanyie F, Harvey RR, Harris JR, Wiegand RE, Gaul L, Desvignes-Kendrick M, Irvin K, Williams I, Hall RL, Herwaldt B, Gray EB, Qvarnstrom Y, Wise ME, Cantu V, Cantey PT, Bosch S, DA Silva AJ, Fields A, Bishop H, Wellman A, Beal J, Wilson N, Fiore AE, Tauxe R, Lance S, Slutsker L, Parise M; Multistate Cyclosporiasis Outbreak Investigation Team. 2013 multistate outbreaks of Cyclospora cayetanensis infections associated with fresh produce: focus on the Texas investigations. Epidemiol Infect 2015; 143(16): 3451–3458
https://doi.org/10.1017/S0950268815000370
pmid: 25865140
|
35 |
El Baidouri F, Diancourt L, Berry V, Chevenet F, Pratlong F, Marty P, Ravel C. Genetic structure and evolution of the Leishmania genus in Africa and Eurasia: what does MLSA tell us. PLoS Negl Trop Dis 2013; 7(6): e2255
https://doi.org/10.1371/journal.pntd.0002255
pmid: 23785530
|
36 |
Li N, Xiao L, Cama VA, Ortega Y, Gilman RH, Guo M, Feng Y. Genetic recombination and Cryptosporidium hominis virulent subtype IbA10G2. Emerg Infect Dis 2013; 19(10): 1573–1582
https://doi.org/10.3201/eid1910.121361
pmid: 24050210
|
37 |
Qvarnstrom Y, Wei-Pridgeon Y, Li W, Nascimento FS, Bishop HS, Herwaldt BL, Moss DM, Nayak V, Srinivasamoorthy G, Sheth M, Arrowood MJ. Draft genome sequences from Cyclospora cayetanensis oocysts purified from a human stool sample. Genome Announc 2015; 3(6): e01324–e01315
https://doi.org/10.1128/genomeA.01324-15
pmid: 26586880
|
38 |
Guo Y, Roellig DM, Li N, Tang K, Frace M, Ortega Y, Arrowood MJ, Feng Y, Qvarnstrom Y, Wang L, Moss DM, Zhang L, Xiao L. Multilocus sequence typing tool for Cyclospora cayetanensis. Emerg Infect Dis 2016; 22(8): 1464–1467
https://doi.org/10.3201/eid2208.150696
pmid: 27433881
|
39 |
Cinar HN, Gopinath G, Jarvis K, Murphy HR. The complete mitochondrial genome of the foodborne parasitic pathogen Cyclospora cayetanensis. PLoS One 2015; 10(6): e0128645
https://doi.org/10.1371/journal.pone.0128645
pmid: 26042787
|
40 |
Ogedengbe ME, Qvarnstrom Y, da Silva AJ, Arrowood MJ, Barta JR. A linear mitochondrial genome of Cyclospora cayetanensis (Eimeriidae, Eucoccidiorida, Coccidiasina, Apicomplexa) suggests the ancestral start position within mitochondrial genomes of eimeriid coccidia. Int J Parasitol 2015; 45(6): 361–365
https://doi.org/10.1016/j.ijpara.2015.02.006
pmid: 25812835
|
41 |
Preston MD, Campino S, Assefa SA, Echeverry DF, Ocholla H, Amambua-Ngwa A, Stewart LB, Conway DJ, Borrmann S, Michon P, Zongo I, Ouédraogo JB, Djimde AA, Doumbo OK, Nosten F, Pain A, Bousema T, Drakeley CJ, Fairhurst RM, Sutherland CJ, Roper C, Clark TG. A barcode of organellar genome polymorphisms identifies the geographic origin of Plasmodium falciparum strains. Nat Commun 2014; 5: 4052
https://doi.org/10.1038/ncomms5052
pmid: 24923250
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|