Global Burden of Cyclospora cayetanensis Infection and Associated Risk Factors in People Living with HIV and/or AIDS
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search Strategy and Selection Criteria
2.2. Assessment of Risk of Bias and Quality in the Included Studies
2.3. Data Extraction and Analysis
2.4. Meta-Analysis
3. Result
3.1. Search Results
3.2. Characteristics of Studies
3.3. Statistical Analysis
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Arora, D.; Arora, B. AIDS-associated parasitic diarrhoea. Indian J. Med. Microbiol. 2009, 27, 185–190. [Google Scholar] [CrossRef] [PubMed]
- Uzairue, L.I.; Oghena, M.; Ikede, R.E.; Aguda, O.N.; Adebisi, Y.A.; Lucero-Prisno, D.E., III. Prevalence, risk factors and impact of cellular immunity on intestinal parasitosis among people living with HIV at Auchi, Edo State, Nigeria. Int. J. STD AIDS 2021, 32, 1106–1113. [Google Scholar] [CrossRef] [PubMed]
- UNAIDS DATA 2021. Available online: https://www.unaids.org/sites/default/files/media_asset/JC3032_AIDS_Data_book_2021_En.pdf (accessed on 12 December 2021).
- Batista, F.S.; Miranda, L.d.S.; Silva, M.B.d.O.; Taborda, R.L.M.; Soares, M.C.F.; Matos, N.B. Chronic Cystoisospora belli infection in an HIV/AIDS patient treated at the specialized assistance service in Porto Velho County-Rondônia. Rev. Da Soc. Bras. De Med. Trop. 2019, 52, e20180204. [Google Scholar] [CrossRef] [PubMed]
- Siddiqui, U.; Bini, E.J.; Chandarana, K.; Leong, J.; Ramsetty, S.; Schiliro, D.; Poles, M. Prevalence and impact of diarrhea on health-related quality of life in HIV-infected patients in the era of highly active antiretroviral therapy. J. Clin. Gastroenterol. 2007, 41, 484–490. [Google Scholar] [CrossRef]
- Dikman, A.E.; Schonfeld, E.; Srisarajivakul, N.C.; Poles, M.A. Human immunodeficiency virus-associated diarrhea: Still an issue in the era of antiretroviral therapy. Dig. Dis. Sci. 2015, 60, 2236–2245. [Google Scholar] [CrossRef] [Green Version]
- Agholi, M.; Shahabadi, S.N.; Motazedian, M.H.; Hatam, G.R. Prevalence of enteric protozoan oocysts with special reference to Sarcocystis cruzi among fecal samples of diarrheic immunodeficient patients in Iran. Korean J. Parasitol. 2016, 54, 339. [Google Scholar] [CrossRef] [Green Version]
- Opoku, Y.K.; Boampong, J.N.; Ayi, I.; Kwakye-Nuako, G.; Obiri-Yeboah, D.; Koranteng, H.; Ghartey-Kwansah, G.; Asare, K.K. Socio-Behavioral Risk Factors Associated with Cryptosporidiosis in HIV/AIDS Patients Visiting the HIV Referral Clinic at Cape Coast Teaching Hospital, Ghana. Open AIDS J. 2018, 12, 106. [Google Scholar] [CrossRef] [Green Version]
- Barazesh, A.; Fouladvand, M.; Tahmasebi, R.; Heydari, A.; Kooshesh, F. Prevalence of intestinal parasitic infections among primary school children in Bushehr, Iran. Avicenna J. Clin. Microbiol. Infect. 2016, 4, 34335. [Google Scholar] [CrossRef]
- Saki, J.; Amraee, D. Prevalence of intestinal parasites among the rural primary school students in the west of Ahvaz county, Iran, 2015. Jentashapir J. Health Res. 2017, 8, e40326. [Google Scholar] [CrossRef] [Green Version]
- Chacín-Bonilla, L. Epidemiology of Cyclospora cayetanensis: A review focusing in endemic areas. Acta Trop. 2010, 115, 181–193. [Google Scholar] [CrossRef]
- Wiwanitkit, V. Intestinal parasite infestation in HIV infected patients. Curr. HIV Res. 2006, 4, 87–96. [Google Scholar] [CrossRef] [PubMed]
- Naganathan, T.; O’Connor, A.; Sargeant, J.M.; Shapiro, K.; Totton, S.; Winder, C.; Greer, A.L. The prevalence of Cyclospora cayetanensis in water: A systematic review and meta-analysis. Epidemiol. Infect. 2022, 150, e15. [Google Scholar] [CrossRef]
- Dubey, J.P.; Almeria, S.; Mowery, J.; Fortes, J. Endogenous developmental cycle of the human coccidian Cyclospora cayetanensis. J. Parasitol. 2020, 106, 295–307. [Google Scholar] [CrossRef] [PubMed]
- Almeria, S.; Cinar, H.N.; Dubey, J.P. Cyclospora cayetanensis and cyclosporiasis: An update. Microorganisms 2019, 7, 317. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, H.; Zhou, Y.; Tang, W. Maintaining HIV care during the COVID-19 pandemic. Lancet HIV 2020, 7, e308–e309. [Google Scholar] [CrossRef]
- Moher, D.; Shamseer, L.; Clarke, M.; Ghersi, D.; Liberati, A.; Petticrew, M.; Shekelle, P.; Stewart, L.A. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst. Rev. 2015, 4, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Joanna Briggs Institute. Joanna Briggs Institute Reviewers’ Manual 2014; The University of Adelaide: Adelaide, Australia, 2014. [Google Scholar]
- Agholi, M.; Hatam, G.R.; Motazedian, M.H. HIV/AIDS-associated opportunistic protozoal diarrhea. AIDS Res. Hum. Retrovir. 2013, 29, 35–41. [Google Scholar] [CrossRef] [Green Version]
- Uysal, H.K.; Adas, G.T.; Atalik, K.; Altiparmak, S.; Akgul, O.; Saribas, S.; Gurcan, M.; Yuksel, P.; Yildirmak, T.; Kocazeybek, B. The prevalence of Cyclospora cayetanensis and Cryptosporidium spp. in Turkish patients infected with HIV-1. Acta Parasitol. 2017, 62, 557–564. [Google Scholar] [CrossRef]
- Masoumi-Asl, H.; Khanaliha, K.; Bokharaei-Salim, F.; Esteghamati, A.; Kalantari, S.; Hosseinyrad, M. Enteric opportunistic infection and the impact of antiretroviral therapy among hiv/aids patients from Tehran, Iran. Iran. J. Public Health 2019, 48, 730. [Google Scholar] [CrossRef]
- Pape, J.W.; Verdier, R.-I.; Boncy, M.; Boncy, J.; Johnson, W.D. Cyclospora infection in adults infected with HIV: Clinical manifestations, treatment, and prophylaxis. Ann. Intern. Med. 1994, 121, 654–657. [Google Scholar] [CrossRef]
- Sifuentes-Osornio, J.; Porras-Cortés, G.; Bendall, R.P.; Morales-Villarreal, F.; Reyes-Terán, G.; Ruiz-Palacios, G.M. Cyclospora cayetanensis infection in patients with and without AIDS: Biliary disease as another clinical manifestation. Clin. Infect. Dis. 1995, 21, 1092–1097. [Google Scholar] [CrossRef] [PubMed]
- Manatsathit, S.; Tansupasawasdikul, S.; Wanachiwanawin, D.; Setawarin, S.; Suwanagool, P.; Prakasvejakit, S.; Leelakusolwong, S.; Eampokalap, B.; Kachintorn, U. Causes of chronic diarrhea in patients with AIDS in Thailand: A prospective clinical and microbiological study. J. Gastroenterol. 1996, 31, 533–537. [Google Scholar] [CrossRef] [PubMed]
- Germani, Y.; Minssart, P.; Vohito, M.; Yassibanda, S.; Glaziou, P.; Hocquet, D.; Berthelemy, P.; Morvan, J. Etiologies of acute, persistent, and dysenteric diarrheas in adults in Bangui, Central African Republic, in relation to human immunodeficiency virus serostatus. Am. J. Trop. Med. Hyg. 1998, 59, 1008–1014. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lindo, J.F.; Dubon, J.M.; Ager, A.L.; De Gourville, E.M.; Solo-Gabriele, H.; Klaskala, W.I.; Baum, M.K.; Palmer, C.J. Intestinal parasitic infections in human immunodeficiency virus (HIV)-positive and HIV-negative individuals in San Pedro Sula, Honduras. Am. J. Trop. Med. Hyg. 1998, 58, 431–435. [Google Scholar] [CrossRef]
- Cegielski, J.P.; Ortega, Y.R.; McKee, S.; Madden, J.F.; Gaido, L.; Schwartz, D.A.; Manji, K.; Jorgensen, A.F.; Miller, S.E.; Pulipaka, U.P. Cryptosporidium, Enterocytozoon, and Cyclospora infections in pediatric and adult patients with diarrhea in Tanzania. Clin. Infect. Dis. 1999, 28, 314–321. [Google Scholar] [CrossRef] [Green Version]
- Escobedo, A.A.; Núñez, F.A. Prevalence of intestinal parasites in Cuban acquired immunodeficiency syndrome (AIDS) patients. Acta Trop. 1999, 72, 125–130. [Google Scholar] [CrossRef]
- Gumbo, T.; Sarbah, S.; Gangaidzo, I.T.; Ortega, Y.; Sterling, C.R.; Carville, A.; Tzipori, S.; Wiest, P.M. Intestinal parasites in patients with diarrhea and human immunodeficiency virus infection in Zimbabwe. Aids 1999, 13, 819–821. [Google Scholar] [CrossRef]
- Mukhopadhya, A.; Ramakrishna, B.; Kang, G.; Pulimood, A.B.; Mathan, M.M.; Zachariah, A.; Mathai, D.C. Enteric pathogens in southern Indian HIV-infected patients with & without diarrhoea. Indian J. Med. Res. 1999, 109, 85–89. [Google Scholar]
- Chacin-Bonilla, L.; Estévez, J.; Monsalve, F.; Quijada, L. Cyclospora cayetanensis infections among diarrheal patients from Venezuela. Am. J. Trop. Med. Hyg. 2001, 65, 351–354. [Google Scholar] [CrossRef] [Green Version]
- Pratdesaba, R.A.; González, M.; Piedrasanta, E.; Mérida, C.; Contreras, K.; Vela, C.; Culajay, F.; Flores, L.; Torres, O. Cyclospora cayetanensis in three populations at risk in Guatemala. J. Clin. Microbiol. 2001, 39, 2951–2953. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.S.; Ananthan, S.; Lakshmi, P. Intestinal parasitic infection in HIV infected patients with diarrhoea in Chennai. Indian J. Med. Microbiol. 2002, 20, 88. [Google Scholar] [PubMed]
- Mohandas, K.; Sehgal, R.; Sud, A.; Malla, N. Prevalence of intestinal parasitic pathogens in HIV-seropositive individuals in Northern India. Jpn. J. Infect. Dis. 2002, 55, 83–84. [Google Scholar] [PubMed]
- Wang, K.-X.; Li, C.-P.; Wang, J.; Tian, Y. Cyclospora cayetanensis in Anhui, China. World J. Gastroenterol. 2002, 8, 1144. [Google Scholar] [CrossRef] [PubMed]
- Capó de Paz, V.; Barrero Brínguez, M.; Velázquez Viamonte, B.; Luzardo Suárez, C.; Martínez Rodríguez, A.; Alujas Martínez, Z. Diagnóstico de coccidias y microsporas en muestras de heces diarreicas de pacientes cubanos seropositivos al VIH: Primer reporte de microsporas en Cuba. Rev. Cuba. De Med. Trop. 2003, 55, 14–18. [Google Scholar]
- Chacin-Bonilla, L.; Panunzio, A.P.; Monsalve-Castillo, F.M.; Parra-Cepeda, I.E.; Martinez, R. Microsporidiosis in Venezuela: Prevalence of intestinal microsporidiosis and its contribution to diarrhea in a group of Human Immunodeficiency Virus–infected patients from Zulia State. Am. J. Trop. Med. Hyg. 2006, 74, 482–486. [Google Scholar] [CrossRef] [Green Version]
- Sarfati, C.; Bourgeois, A.; Menotti, J.; Liegeois, F.; Moyou-Somo, R.; Delaporte, E.; Derouin, F.; Ngole, E.M.; Molina, J.-M. Prevalence of intestinal parasites including microsporidia in human immunodeficiency virus–infected adults in Cameroon: A cross-sectional study. Am. J. Trop. Med. Hyg. 2006, 74, 162–164. [Google Scholar] [CrossRef]
- Becker, M.L.; Cohen, C.R.; Cheang, M.; Washington, R.G.; Blanchard, J.F.; Moses, S. Diarrheal disease among HIV-infected adults in Karnataka, India: Evaluation of risk factors and etiology. Am. J. Trop. Med. Hyg. 2007, 76, 718–722. [Google Scholar] [CrossRef]
- Kaminsky, R.G.; Stovall, M.; Mayer, M.; Martin, A.D.; Bowers, L.C.; Didier, E.S. Microsporidia intestinales en pacientes viviendo con SIDA en Honduras. Rev Méd Hondur 2007, 75, 116–123. [Google Scholar]
- Gupta, S.; Narang, S.; Nunavath, V.; Singh, S. Chronic diarrhoea in HIV patients: Prevalence of coccidian parasites. Indian J. Med. Microbiol. 2008, 26, 172–175. [Google Scholar] [CrossRef]
- Raccurt, C.P.; Fouché, B.; Agnamey, P.; Menotti, J.; Chouaki, T.; Totet, A.; Pape, J.W. Presence of Enterocytozoon bieneusi associated with intestinal coccidia in patients with chronic diarrhea visiting an HIV center in Haiti. Am. J. Trop. Med. Hyg. 2008, 79, 579–580. [Google Scholar] [CrossRef] [Green Version]
- Tuli, L.; Gulati, A.K.; Sundar, S.; Mohapatra, T.M. Correlation between CD4 counts of HIV patients and enteric protozoan in different seasons–An experience of a tertiary care hospital in Varanasi (India). BMC Gastroenterol. 2008, 8, 36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kulkarni, S.; Kairon, R.; Sane, S.; Padmawar, P.; Kale, V.; Thakar, M.; Mehendale, S.; Risbud, A. Opportunistic parasitic infections in HIV/AIDS patients presenting with diarrhoea by the level of immunesuppression. Indian J. Med. Res. 2009, 130, 63. [Google Scholar] [PubMed]
- Kurniawan, A.; Karyadi, T.; Dwintasari, S.; Sari, I.P.; Yunihastuti, E.; Djauzi, S.; Smith, H. Intestinal parasitic infections in HIV/AIDS patients presenting with diarrhoea in Jakarta, Indonesia. Trans. R. Soc. Trop. Med. Hyg. 2009, 103, 892–898. [Google Scholar] [CrossRef]
- Saksirisampant, W.; Prownebon, J.; Saksirisampant, P.; Mungthin, M.; Siripatanapipong, S.; Leelayoova, S. Intestinal parasitic infections: Prevalences in HIV/AIDS patients in a Thai AIDS-care centre. Ann. Trop. Med. Parasitol. 2009, 103, 573–581. [Google Scholar] [CrossRef] [PubMed]
- Viriyavejakul, P.; Nintasen, R.; Punsawad, C.; Chaisri, U.; Punpoowong, B.; Riganti, M. High prevalence of Microsporidium infection in HIV-infected patients. Southeast Asian J. Trop. Med. Public Health 2009, 40, 223. [Google Scholar] [PubMed]
- Babatunde, S.; Salami, A.; Fabiyi, J.; Agbede, O.; Desalu, O. Prevalence of intestinal parasitic infestation in HIV seropositive and seronegative patients in Ilorin, Nigeria. Ann. Afr. Med. 2010, 9, 123–128. [Google Scholar] [PubMed] [Green Version]
- Asma, I.; Johari, S.; Sim, B.L.H.; Lim, Y.A.L. How common is intestinal parasitism in HIV-infected patients in Malaysia? Trop. Biomed. 2011, 28, 400–410. [Google Scholar] [PubMed]
- Mathur, M.K.; Verma, A.K.; Makwana, G.E.; Sinha, M. Study of opportunistic intestinal parasitic infections in human immunodeficiency virus/acquired immunodeficiency syndrome patients. J. Glob. Infect. Dis. 2013, 5, 164. [Google Scholar] [CrossRef]
- Rivero-Rodríguez, Z.; Hernández, A.; Bracho, Á.; Salazar, S.; Villalobos, R. Prevalence of intestinal microsporidia and other intestinal parasites in hiv positive patients from Maracaibo, Venezuela. Biomedica 2013, 33, 538–545. [Google Scholar]
- Tiwari, B.R.; Ghimire, P.; Malla, S.; Sharma, B.; Karki, S. Intestinal parasitic infection among the HIV-infected patients in Nepal. J. Infect. Dev. Ctries. 2013, 7, 550–555. [Google Scholar] [CrossRef] [Green Version]
- Ahmed, N.H.; Chowdhary, A. Pattern of co-infection by enteric pathogenic parasites among HIV sero-positive individuals in a Tertiary Care Hospital, Mumbai, India. Indian J. Sex. Transm. Dis. AIDS 2015, 36, 40. [Google Scholar] [PubMed] [Green Version]
- Nsagha, D.S.; Njunda, A.L.; Assob, N.J.C.; Ayima, C.W.; Tanue, E.A.; Kwenti, T.E. Intestinal parasitic infections in relation to CD4+ T cell counts and diarrhea in HIV/AIDS patients with or without antiretroviral therapy in Cameroon. BMC Infect. Dis. 2015, 16, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shah, S.; Kongre, V.; Kumar, V.; Bharadwaj, R. A study of parasitic and bacterial pathogens associated with diarrhea in HIV-positive patients. Cureus 2016, 8, e807. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Swathirajan, C.R.; Vignesh, R.; Pradeep, A.; Solomon, S.S.; Solomon, S.; Balakrishnan, P. Occurrence of enteric parasitic infections among HIV-infected individuals and its relation to CD4 T-cell counts with a special emphasis on coccidian parasites at a tertiary care centre in South India. Indian J. Med. Microbiol. 2017, 35, 37–40. [Google Scholar] [CrossRef] [PubMed]
- Alemu, G.; Alelign, D.; Abossie, A. Prevalence of opportunistic intestinal parasites and associated factors among HIV patients while receiving ART at Arba Minch Hospital in southern Ethiopia: A cross-sectional study. Ethiop. J. Health Sci. 2018, 28, 147–156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zorbozan, O.; Quliyeva, G.; Tunalı, V.; Özbilgin, A.; Turgay, N.; Gökengin, A.D. HIV ile Enfekte Olguların Bağırsak Protozoonları Açısından Retrospektif Olarak İncelenmesi. Turk. Parazitol Derg 2018, 42, 187–190. [Google Scholar] [CrossRef]
- Rodríguez-Pérez, E.G.; Arce-Mendoza, A.Y.; Montes-Zapata, É.I.; Limón, A.; Rodríguez, L.É.; Escandón-Vargas, K. Opportunistic intestinal parasites in immunocompromised patients from a tertiary hospital in Monterrey, Mexico. Le Infez. Med. Riv. Period. Di Eziologia Epidemiol. Diagn. Clin. E Ter. Delle Patol. Infett. 2019, 27, 168–174. [Google Scholar]
- Udeh, E.O.; Obiezue, R.; Okafor, F.; Ikele, C.; Okoye, I.; Otuu, C.A. Gastrointestinal parasitic infections and immunological status of HIV/AIDS coinfected individuals in Nigeria. Ann. Glob. Health 2019, 85, 99. [Google Scholar] [CrossRef]
- Namaji, M.A.A.S.; Pathan, S.H.; Balki, A.M. Profile of intestinal parasitic infections in human immunodeficiency virus/acquired immunodeficiency syndrome patients in Northeast India. Indian J. Sex. Transm. Dis. AIDS 2020, 41, 93. [Google Scholar] [CrossRef]
- Chacín-Bonilla, L. Importancia del contacto con la tierra en la transmisión de la ciclosporosis. Investig. Clínica 2010, 51, 441–443. [Google Scholar]
- Burstein Alva, S. Ciclosporosis: Una parasitosis emergente (II). Diagnóstico Microbiológico mediante una nueva técnica de coloración. Rev. De Gastroenterol. Del Perú 2005, 25, 336–340. [Google Scholar]
- Fletcher, S.M.; Stark, D.; Ellis, J. Prevalence of gastrointestinal pathogens in Sub-Saharan Africa: Systematic review and meta-analysis. J. Public Health Afr. 2011, 2, e30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, J.; Wang, R.; Chen, Y.; Xiao, L.; Zhang, L. Cyclospora cayetanensis infection in humans: Biological characteristics, clinical features, epidemiology, detection method and treatment. Parasitology 2020, 147, 160–170. [Google Scholar] [CrossRef] [PubMed]
- Brenchley, J.M.; Douek, D. HIV infection and the gastrointestinal immune system. Mucosal Immunol. 2008, 1, 23–30. [Google Scholar] [CrossRef] [PubMed]
- Jagai, J.S.; Castronovo, D.A.; Monchak, J.; Naumova, E.N. Seasonality of cryptosporidiosis: A meta-analysis approach. Environ. Res. 2009, 109, 465–478. [Google Scholar] [CrossRef] [Green Version]
- Lobo, M.L.; Xiao, L.; Antunes, F.; Matos, O. Microsporidia as emerging pathogens and the implication for public health: A 10-year study on HIV-positive and-negative patients. Int. J. Parasitol. 2012, 42, 197–205. [Google Scholar] [CrossRef]
- Weinreich, F.; Hahn, A.; Eberhardt, K.A.; Feldt, T.; Sarfo, F.S.; Di Cristanziano, V.; Frickmann, H.; Loderstädt, U. Comparison of Three Real-Time PCR Assays for the Detection of Cyclospora cayetanensis in Stool Samples Targeting the 18S rRNA Gene and the hsp70 Gene. Pathogens 2022, 11, 165. [Google Scholar] [CrossRef]
NO | First Author | Q1 | Q2 | Q3 | Q4 | Q5 | Q6 | Q7 | Q8 | Q9 | Score |
---|---|---|---|---|---|---|---|---|---|---|---|
1 | J.W. Pape | | | | | | | | | | 4 |
2 | J. Sifuentes | | | | | | | | | | 4 |
3 | S. Manatsathit | | | | | | | | | | 5 |
4 | Y. Germani | | | | | | | | | | 6 |
5 | J.F. Lindo | | | | | | | | | | 4 |
6 | J.P. Cegielski | | | | | | | | | | 6 |
7 | A. Escobedo | | | | | | | | | | 5 |
8 | T. Gumbo | | | | | | | | | | 7 |
9 | A. Mukhopadhya | | | | | | | | | | 5 |
10 | L. Chacin-Bonilla | | | | | | | | | | 7 |
11 | R.A. Pratdesaba | | | | | | | | | | 4 |
12 | S.S. Kumar | | | | | | | | | | 4 |
13 | K. Mohandas | | | | | | | | | | 6 |
14 | K.-X. Wang | | | | | | | | | | 6 |
15 | V. Capó de Paz | | | | | | | | | | 6 |
16 | L. Chacin-Bonilla | | | | | | | | | | 7 |
17 | C. Sarfati | | | | | | | | | | 7 |
18 | M.L. Becker | | | | | | | | | | 6 |
19 | R.G. Kaminsky | | | | | | | | | | 5 |
20 | S. Gupta | | | | | | | | | | 6 |
21 | C.P. Raccurt | | | | | | | | | | 6 |
22 | L. Tuli | | | | | | | | | | 9 |
23 | S. Kulkarni | | | | | | | | | | 6 |
24 | A. Kurniawan | | | | | | | | | | 5 |
25 | W. Saksirisampant | | | | | | | | | | 5 |
26 | P. Viriyavejakul | | | | | | | | | | 6 |
27 | S. Babatunde | | | | | | | | | | 7 |
28 | I. Asma | | | | | | | | | | 9 |
29 | M. Agholi | | | | | | | | | | 7 |
30 | M.K. Mathur | | | | | | | | | | 5 |
31 | Z. Rivero-Rodríguez | | | | | | | | | | 5 |
32 | B.R. Tiwari | | | | | | | | | | 9 |
33 | N.H. Ahmed | | | | | | | | | | 9 |
34 | D.S. Nsagha | | | | | | | | | | 7 |
35 | M. Agholi | | | | | | | | | | 5 |
36 | S. Shah | | | | | | | | | | 8 |
37 | C.R. Swathirajan | | | | | | | | | | 6 |
38 | H.K. Uysal | | | | | | | | | | 6 |
39 | G. Alemu | | | | | | | | | | 6 |
40 | Y.K. Opoku | | | | | | | | | | 8 |
41 | O. Zorbozan | | | | | | | | | | 5 |
42 | H. Masoumi-Asl | | | | | | | | | | 7 |
43 | E.G. Rodríguez-Pérez | | | | | | | | | | 5 |
44 | E.O. Udeh | | | | | | | | | | 8 |
45 | M.A.A.S. Namaji | | | | | | | | | | 5 |
NO | First Author | Year | Country | Study Design | No. of Participants/Positive Patients | Mean Age | Diagnostic Method | Patients with Diarrhea | Patients with CD4 <200 | Ref. |
---|---|---|---|---|---|---|---|---|---|---|
1 | J.W. Pape | 1994 | Haiti | Cohort | 450/43 | 24 | Modified Kinyoun acid-fast | 450 | NR | [22] |
2 | J. Sifuentes | 1995 | Mexico City | Cross-sectional | 235/7 | 40.5 | Modified acid-fast | 235 | NR | [23] |
3 | S. Manatsathit | 1996 | Thailand | Prospective study | 45/1 | 35 | Modified acid-fast | 45 | 45 | [24] |
4 | Y. Germani | 1998 | Central African | Case-control | 171/5 | NR | Modified trichrome | 171 | 171 | [25] |
5 | J.F. Lindo | 1998 | Honduras | Cross-sectional | 52/1 | 33.8 | Modified Kinyoun acid-fast | 16 | NR | [26] |
6 | J.P. Cegielski | 1999 | Tanzania | Case-control | 124/1 | NR | Kinyoun and auramine rhodamine | 124 | NR | [27] |
7 | A. Escobedo | 1999 | Cuba | Case-control | 67/2 | 27.9 | Modified Ziehl–Neelsen | NR | NR | [28] |
8 | T. Gumbo | 1999 | Zimbabwe | Prospective study | 88/0 | 33 | Modified acid-fast | 88 | NR | [29] |
9 | A. Mukhopadhya | 1999 | India | Cross-sectional | 111/5 | NR | Safranine-Methylene blue and auramine | 61 | NR | [30] |
10 | L. Chacin-Bonilla | 2001 | Venezuela | Retrospective study | 71/7 | 33.5 | Modified Ziehl–Neelsen | 71 | NR | [31] |
11 | R.A. Pratdesaba | 2001 | Guatemala | Cross-sectional | 157/6 | 32 | Modified acid-fast | NR | NR | [32] |
12 | S.S. Kumar | 2002 | India | Case-control | 152/1 | 40 | Modified Kinyoun acid- fast and Safranin Methylene blue | 102 | NR | [33] |
13 | K. Mohandas | 2002 | Northern India | Cross-sectional | 120/4 | NR | Ziehl–Neelsen | 26 | NR | [34] |
14 | K.-X. Wang | 2002 | China | Case-control | 32/3 | NR | Auramine phenol stain and modified acid-fast | 32 | NR | [35] |
15 | V. Capó de Paz | 2003 | Cuba | Cross-sectional | 170/6 | NR | Ziehl–Neelsen | 170 | NR | [36] |
16 | L. Chacin-Bonilla | 2006 | Venezuela | Case-control | 74/6 | 37.3 ± 5.6 | Modified Ziehl–Neelsen | 74 | NR | [37] |
17 | C. Sarfati | 2006 | Cameroon | Cross-sectional | 154/0 | 36 | Modified Ziehl–Neelsen | 46 | NR | [38] |
18 | M.L. Becker | 2007 | India | Case-control | 153/0 | 32.7 ± 8 | Acid-fast trichrome | 153 | NR | [39] |
19 | R.G. Kaminsky | 2007 | Honduras | Cross-sectional | 56/2 | 32.3 | Acid-fast trichrome | 18 | NR | [40] |
20 | S. Gupta | 2008 | India | Cross-sectional | 113/1 | 33.2 ± 9.72 | Modified acid-fast | 34 | NR | [41] |
21 | C.P. Raccurt | 2008 | Haiti | Cross-sectional | 67/27 | NR | Weber modified trichrome | 67 | NR | [42] |
22 | L. Tuli | 2008 | India | Case-control | 366/88 | 35.5 | Modified acid-fast and modified safranin | 366 | 236 | [43] |
23 | S. Kulkarni | 2009 | India | Cross-sectional | 137/1 | M: 34.6 ± 7.51 F: 33.2 ± 9.95 | Modified acid-fast | 137 | 65 | [44] |
24 | A. Kurniawan | 2009 | Indonesia | Cross-sectional | 318/12 | NR | Modified acid-fast | NR | NR | [45] |
25 | W. Saksirisampant | 2009 | Thailand | Cross-sectional | 90/1 | 39.5 | Modified Ziehl–Neelsen | 71 | NR | [46] |
26 | P. Viriyavejakul | 2009 | Thailand | Cross-sectional | 64/3 | NR | Ziehl–Neelsen | 64 | NR | [47] |
27 | S. Babatunde | 2010 | Nigeria | Cross-sectional | 90/16 | 35 | Modified Ziehl–Neelsen | 90 | 26 | [48] |
28 | I. Asma | 2011 | Malaysia | Cross-sectional | 346/17 | 21.5 | Modified Ziehl–Neelsen | 30 | 189 | [49] |
29 | M. Agholi | 2013 | Iran | Cross-sectional | 356/1 | 37.18 | Acid-fast trichrome stain, nested PCR | 103 | 188 | [19] |
30 | M.K. Mathur | 2013 | India | Retrospective study | 544/12 | 42.5 | Modified Ziehl–Neelsen | 400 | NR | [50] |
31 | Z. Rivero-Rodríguez | 2013 | Venezuela | Cross-sectional | 56/2 | 35 ± 11.95 | Modified Kinyoun acid-fast | 48 | NR | [51] |
32 | B.R. Tiwari | 2013 | Nepal | Cross-sectional | 745/14 | 30 | Modified acid-fast | 248 | 327 | [52] |
33 | N.H. Ahmed | 2015 | India | Cohort | 142/3 | NR | Modified Ziehl–Neelsen’s cold staining | 142 | NR | [53] |
34 | D.S. Nsagha | 2015 | Cameroon | Cross-sectional | 300/11 | 40 | Modified Ziehl–Neelsen | 118 | 76 | [54] |
35 | M. Agholi | 2016 | Iran | Cross-sectional | 387/2 | NR | Modified acid-fast or acid-fast trichrome and semi-nested PCR | 387 | NR | [7] |
36 | S. Shah | 2016 | India | Cross-sectional | 45/2 | 34.5 | Modified Ziehl–Neelsen | 27 | 22 | [55] |
37 | C.R. Swathirajan | 2017 | South India | Cross-sectional | 829/2 | M: 38 F: 33.5 | Modified acid-fast | 829 | NR | [56] |
38 | H.K. Uysal | 2017 | Turkey | Cross-sectional | 115/3 | 41.5 | Ziehl–Neelsen and Kinyoun acid-fast, molecular methods | NR | 11 | [20] |
39 | G. Alemu | 2018 | Ethiopia | Cross-sectional | 220/13 | NR | Modified Ziehl–Neelsen | 21 | 43 | [57] |
40 | Y.K. Opoku | 2018 | Ghana | Cross-sectional | 50/14 | NR | Ziehl–Neelsen | 50 | NR | [8] |
41 | O. Zorbozan | 2018 | Turkey | Prospective study | 65/2 | 41.9 ± 12.4 | Modified acid-fast, Giemsa, Kinyoun | 65 | NR | [58] |
42 | H. Masoumi-Asl | 2019 | Iran | Cross-sectional | 102/1 | NR | Acid-fast and nested PCR | NR | 9 | [21] |
43 | E.G. Rodríguez-Pérez | 2019 | Mexico | Prospective study | 29/0 | 37 | Modified Ziehl–Neelsen, Giemsa and acid-fast trichrome | NR | NR | [59] |
44 | E.O. Udeh | 2019 | Nigeria | Case-control | 891/9 | NR | Ziehl–Neelsen | NR | 3 | [60] |
45 | M. Namaji | 2020 | India | Cross-sectional | 361/7 | NR | Modified acid-fast | 361 | NR | [61] |
Risk Factors | No. of Studies | Categories | OR (95% CI) | p-Value | I2 (Inconsistency) % | Cochran Q | p-Value |
---|---|---|---|---|---|---|---|
Sex | 3 | Male Female | 1.72 (0.79–3.73) | p = 0.1647 | 0 | 2.06 | p = 0.7244 |
Diarrhea | 8 | Yes No | 3.23 (1.38–7.54) | p = 0.0066 | 0 | 4.81 | p = 0.5675 |
CD4 | 10 | <200 cells/mL >200 cells/mL | 4.07 (1.37–12.12) | p = 0.0115 | 74.5 | 35.24 | p < 0.0001 |
HAART | 3 | No Yes | 2.07 (0.29–14.81) | p = 0.4668 | - | 1.57 | p = 0.2101 |
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Ramezanzadeh, S.; Beloukas, A.; Pagheh, A.S.; Rahimi, M.T.; Hosseini, S.A.; Oliveira, S.M.R.; de Lourdes Pereira, M.; Ahmadpour, E. Global Burden of Cyclospora cayetanensis Infection and Associated Risk Factors in People Living with HIV and/or AIDS. Viruses 2022, 14, 1279. https://doi.org/10.3390/v14061279
Ramezanzadeh S, Beloukas A, Pagheh AS, Rahimi MT, Hosseini SA, Oliveira SMR, de Lourdes Pereira M, Ahmadpour E. Global Burden of Cyclospora cayetanensis Infection and Associated Risk Factors in People Living with HIV and/or AIDS. Viruses. 2022; 14(6):1279. https://doi.org/10.3390/v14061279
Chicago/Turabian StyleRamezanzadeh, Saba, Apostolos Beloukas, Abdol Sattar Pagheh, Mohammad Taghi Rahimi, Seyed Abdollah Hosseini, Sonia M. Rodrigues Oliveira, Maria de Lourdes Pereira, and Ehsan Ahmadpour. 2022. "Global Burden of Cyclospora cayetanensis Infection and Associated Risk Factors in People Living with HIV and/or AIDS" Viruses 14, no. 6: 1279. https://doi.org/10.3390/v14061279