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Systematic Review

Global Burden of Cyclospora cayetanensis Infection and Associated Risk Factors in People Living with HIV and/or AIDS

by
Saba Ramezanzadeh
1,2,
Apostolos Beloukas
3,4,
Abdol Sattar Pagheh
5,
Mohammad Taghi Rahimi
6,
Seyed Abdollah Hosseini
7,
Sonia M. Rodrigues Oliveira
8,9,
Maria de Lourdes Pereira
8,10,* and
Ehsan Ahmadpour
1,11,*
1
Infectious and Tropical Diseases Research Center, Tabriz University of Medical Sciences, Tabriz 51666-14766, Iran
2
Department of Parasitology and Mycology, Faculty of Medicine, Tabriz University of Medical Sciences, Tabriz 51666-14766, Iran
3
National AIDS Reference Center of Southern Greece, Department of Public Health Policy, University of West Attica, 11521 Athens, Greece
4
Molecular Microbiology & Immunology Lab, Department of Biomedical Sciences, University of West Attica, 12243 Athens, Greece
5
Infectious Diseases Research Center, Birjand University of Medical Sciences, Birjand 97178-53577, Iran
6
Center for Health Related Social and Behavioral Sciences Research, Shahroud University of Medical Sciences, Shahroud 36147-73955, Iran
7
Department of Parasitology and Mycology, Faculty of Medicine, Mazandaran University of Medical Sciences, Sari 33971-48157, Iran
8
CICECO-Aveiro Institute of Materials, University of Aveiro, 3810-193 Aveiro, Portugal
9
Hunter Medical Research Institute, New Lambton, NSW 2305, Australia
10
Department of Medical Sciences, University of Aveiro, 3810-193 Aveiro, Portugal
11
Immunology Research Center, Tabriz University of Medical Sciences, Tabriz 51666-14766, Iran
 
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Authors to whom correspondence should be addressed.
Viruses 2022, 14(6), 1279; https://doi.org/10.3390/v14061279
Submission received: 26 May 2022 / Revised: 9 June 2022 / Accepted: 10 June 2022 / Published: 12 June 2022
(This article belongs to the Special Issue State-of-the-Art Virus Research in Greece)
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Abstract

:
Cyclospora cayetanensis infections remain one of the most common protozoan opportunistic causes of gastrointestinal diseases and diarrhea among people living with HIV and/or AIDS (PLWHA). This study was conducted to provide a summary of the evidence on the global burden of C. cayetanensis infection and associated risk factors among PLWHA. Scopus, PubMed, Science Direct, and EMBASE were searched up to February 2022. All original peer-reviewed original research articles were considered, including descriptive and cross-sectional studies describing C. cayetanensis in PLWHA. Incoherence and heterogeneity between studies were quantified by I index and Cochran’s Q test. Publication and population bias were assessed with funnel plots and Egger’s asymmetry regression test. All statistical analyses were performed using StatsDirect. The pooled prevalence of C. cayetanensis infection among PLWHA was 3.89% (95% CI, 2.62–5.40). The highest prevalence found in South America was 7.87% and the lowest in Asia 2.77%. In addition, the prevalence of C. cayetanensis was higher in PLWHA compared to healthy individuals. There was a relationship between a higher C. cayetanensis prevalence in PLWHA with a CD4 cell count below 200 cells/mL and people with diarrhea. The results show that PLWHA are more vulnerable to C. cayetanensis infection and emphasizes the need to implement the screening and prophylaxis tailored to the local context. Owing to the serious and significant clinical manifestations of the parasite, an early identification of seropositivity is recommended to initiate prophylaxis between PLWHA with a CD4 count ≤200 cells/mL and PLWHA who do not receive antiviral therapy.

1. Introduction

The upper and lower gastrointestinal (GI) tract plays a critical role in both the clinical manifestations and pathogenesis of HIV infection. People living with HIV and/or AIDS (PLWHA) are more vulnerable to a variety of opportunistic infections, including gastrointestinal parasitosis [1,2]. Recently, the UNAIDS report estimated that there would be over thirty-eight million PLWHA at the end of 2020 [3]. More than half of immunocompromised PLWHA experience diarrheas that can cause significant morbidity, contributing negatively to the quality of life and to adherence to antiretroviral therapy (ART). This may be due to a multitude of etiologies from infectious pathogens to malignancy to medications [4,5,6]. Over the past decade, due to the unprecedented increase in the use of ART, the incidence of diarrhea from opportunistic infections has decreased [6]; however, it remains a remarkable threat. Opportunistic infectious pathogens that cause diarrhea in PLWHA span a variety of bacteria, fungi, viruses, and parasites. The latter include Toxoplasma, Cryptosporidium, Cystoisospora, and Cyclospora genera that cause moderate to severe diseases [7,8]. Parasitic infections and HIV interact, and parasitic infections may activate the proliferation of HIV and accelerate the progression of the disease from HIV to AIDS. PLWHA with CD4 counts below 200 cells/mL are more prone to GI parasitic infections and to develop disease complications [9]. Apart from diarrhea, GI parasitic infections in immunocompromised PLWHA can cause symptoms such as abdominal pain, fever and chills, muscle aches, eosinophilia, frequent urination and hematuria, clinical manifestations of the central nervous system, weight loss, and transient pneumonia and, in the case of advanced HIV disease, can lead to death [5,10]. Cyclospora cayetanensis is a microscopic food- and waterborne coccidian parasite that is endemic in tropical and subtropical regions [11,12,13,14]. C. cayetanensis infection occurs by ingesting of sporulated oocysts, which are the infective form of the parasite. An infected person sheds unsporulated (immature, non-infective) Cyclospora oocysts in the feces. Oocysts must be sporulated at a temperature of 25–30 °C for at least 1–2 weeks to become infective. Therefore, direct person-to-person transmission is almost impossible, as is transmission via ingestion of newly contaminated food or water. It is thought that the main cause of the spread of C. cayetanensis infection is by ingesting sporulated oocysts from contaminated water and food and lack of hygiene. Clinical manifestations are limited in immunocompetent people but cause chronic watery diarrhea and severe GI damage in immunocompromised patients [15]. There are very limited data on the prevalence of this parasite in PLWHA, and due to the COVID-19 pandemic, we are seeing an increase in the number of immunocompromised patients [16]. Thus, further research will be required to fill this gap of knowledge. Therefore, we conducted a systematic review study to assess the burden of C. cayetanensis parasitosis in PLWHA to implement better prevention and treatment strategies.

2. Materials and Methods

2.1. Search Strategy and Selection Criteria

This systematic review was conducted according to the principles outlined in the PRISMA statement (Preferred Reporting Items for Systematic and Meta-Analysis) and PRISMA-P checklist [17]. Search methods attempted to identify all relevant studies regardless of language, date of publication, or publication status. Two independent investigators (A.S.P., S.R.) systematically searched electronic databases, including PubMed, ProQuest, Scopus, Science Direct, and Google Scholar. The final search was conducted up to 28 February 2022. Keywords used for the searches were Cyclospora, Cyclospora cayetanensis, Cyclosporiasis, intestinal parasite, immunocompromised patients, HIV, AIDS, epidemiology, and prevalence.
Studies were included if they met the following criteria: (1) papers published in the English language, (2) articles presenting people living with HIV and/or AIDS, and (3) articles showing the age of patients and the geographical area. We also excluded studies if they were case reports, letter to the editor, reviews, animal studies, or duplicates. After removing duplicates using the Endnote program (www.endnote.com, accessed on 14 February 2022), titles and abstracts of unique papers identified in the search results were independently screened by two authors (A.S.P., S.R.) according to inclusion and exclusion criteria. Full texts were retrieved for all citations marked as “included”. Where appropriate, multiple reports on the same study were identified and merged. Disagreements were resolved by discussion or with the assistance of a third author (E.R.). We also used the PRISMA Flow Diagram. Authors were contacted where data were unclear. Individual patient-level data were sought.

2.2. Assessment of Risk of Bias and Quality in the Included Studies

Two authors independently assessed the quality of the studies using the JBI (Joanna Briggs Institute) checklist [18]. These tools rate the quality of selection, measurement, and comparability and give a score to the studies (maximum of 9). This tool comprised nine items with four options: “yes”, “no”, “unclear”, and “not applicable”. “Yes” answers were used to calculate the final score of each article.

2.3. Data Extraction and Analysis

A study-level data extraction table was designed, piloted, and modified appropriately using Microsoft Excel (Microsoft Office®, 2019 version). The data extraction form included the following fields: year of publication, region, study design, sample sizes, gender, number of people with diarrhea, CD4 counts of patients, prevalence of C. cayetanensis, diagnostic method, interfering factor, and HAART. Duplicate data were noted and excluded.

2.4. Meta-Analysis

The primary aim was to assess the global prevalence of Cyclospora parasitosis in PLWHA. The statistical heterogeneity between studies was assessed using Cochran’s and I2 tests. For meta-analysis purposes, a random-effects model was used. The meta-analysis was completed with the trial version of the StatsDirect statistical software (www.statsdirect.com, accessed on 7 March 2022). A forest plot was applied to show the heterogeneity between studies. It showed proportions of individual studies and total prevalence of C. cayetanensis.

3. Result

3.1. Search Results

Our preliminary search of five scientific databases yielded 998 records. From that, 402 were excluded as duplicate records. Of the 596 remaining records, 293 articles were excluded after review of titles and abstracts. These included 6 review articles, 19 case reports, and 248 irrelevant articles. Then, the full text of 303 articles was evaluated, and 258 studies did not meet our inclusion criteria. Finally, we retrieved 45 full texts to assess the eligibility for inclusion, and these were included in the systematic review and meta-analysis. A PRISMA diagram of the screening process is depicted in Figure 1.

3.2. Characteristics of Studies

The quality of the studies was assessed using the JBI critical appraisal checklist. None of the studies assessed for quality by the JBI checklist were excluded due to lack of merit. As a result of the reviews, of the 45 articles: two articles received 3 points, four articles received 4 points, twelve articles received 5 points, thirteen articles received 6 points, eight articles received 7 points, three articles received 8 points, and four articles received 9 points. In total, the score was 6 (moderate quality) (Table 1). In total, 9310 PLWHA were included in our study. The identified studies were conducted in 21 countries across four continents. Studies selected included reports from North America (20%, 9/45), South America (6.6%, 3/45), Asia (53.3%, 24/45), and Africa (20%, 9/45). All of these were conducted between 1994 and 2022.
Q1: Was the sample frame appropriate to address the target population?
Q2: Were study participants sampled in an appropriate way?
Q3: Was the sample size adequate?
Q4: Were the study subjects and the setting described in detail?
Q5: Was the data analysis conducted with sufficient coverage of the identified sample?
Q6: Were valid methods used for the identification of the condition?
Q7: Was the condition measured in a standard, reliable way for all participants?
Q8: Was there appropriate statistical analysis?
Q9: Was the response rate adequate, and if not, was the low response rate managed appropriately?
Europe and Oceania had no study meeting the inclusion criteria. Study types included cross-sectional (62.2%, 28/45), case-control studies (20%, 9/45), retrospective (13.3%, 6/45), and cohort (4.4%, 2/45) studies. In all included studies (100%, 45/45), staining was used for the diagnosis of C. cayetanensis infection and, in four included studies (8.8%, 4/45), molecular methods (Table 2). A number of studies used several methods at the same time to confirm the presence of C. cayetanensis [7,19,20,21]. The overall male-to-female ratio was 59.35% to 40.64% (M:F = 1.46:1) among all PLWHA. In total, 44.7% (485/1085) of PLWHA had diagnosed diarrhea, 34% (1130/3317) had CD4 counts <200 cells/mL, and 74.5% (444/596) were on highly active antiretroviral therapy (HAART), while 55.36% (821/1483) received antibiotics.

3.3. Statistical Analysis

The estimated global prevalence of Cyclospora parasitosis in PLWHA ranged from 0.0% to 40.3%. Of 9310 samples, 364 were infected with C. cayetanensis. The estimated global pooled prevalence of C. cayetanensis infection in PLWHA using the random effects model for meta-analysis was 3.89% (95% CI, 2.62–5.40(. The prevalence of the parasite in North America, South America, Asia, and Africa was estimated at 6.22% (95% CI 2.61–11.23, 94/1283), 7.87% (95% CI, 4.58–11.95, 15/201), 2.77% (95% CI, 1.44–4.53, 576/186), and 4.2% (95% CI, 1.55–8.06, 69/2088), respectively. The geographic distribution of C. cayetanensis infection in PLWHA is shown in Figure 2. The pooled prevalence of C. cayetanensis infection in men compared to women (OR = 1.72, 95% CI, 0.79–3.73, p = 0.1647) was also estimated. Furthermore, the pooled prevalence of C. cayetanensis in PLWHA with diarrhea compared with/without diarrhea was estimated (OR = 3.23, 95% CI, 1.38–7.54, p = 0.0066). The pooled prevalence of C. cayetanensis in patients with a CD4 counts <200 cells/mL compared to patients with a CD4 count of more than 200 cells/mL was estimated (OR = 4.07, 95% CI, 1.37–12.12, p = 0.0115). Moreover, the pooled prevalence of C. cayetanensis in patients who did not receive HAART compared with patients with HAART was estimated (OR = 2.07, 95% CI, 0.29–14.81, p = 0.4668) (Table 3), and the pooled prevalence of C. cayetanensis in PLWHA compared to people without HIV was estimated (OR = 4.36, 95% CI, 2–9.48, p = 0.0002). There was a broad difference in the prevalence rate between various studies. Furthermore, the Cochran’s Q statistic was (Q = 506.06, df = 44, p < 0.000, I2 = 91.3%, 95% CI, 89.6%–92.6%) (Figure 3). Inspection of the bias assessment plot showed publication bias, and a statistically significant Egger’s regression suggests the possibility of publication bias (Figure 4).

4. Discussion

This systematic review and meta-analysis provide comprehensive data on the global prevalence of C. cayetanensis in PLWHA. Our findings highlight the high global burden on PLWHA. The global pooled prevalence of C. cayetanensis was 3.89% and was significantly higher in people with diarrhea, OR = 3.23 (95% CI, 1.38–7.54). There were contradictory studies regarding to the prevalence of the parasite, especially in immunocompromised individuals. A study by Chacín-Bonilla reported the rate of C. cayetanensis infection up to 2010 [11], with a prevalence varying from 0% to 13% in 47,642 apparently immunocompetent individuals, most with diarrhea. Furthermore, the prevalence rate in matched asymptomatic controls varied from 0% to 4.2% among 3340 immunocompromised patients, mostly HIV/AIDS patients with diarrhea, whose prevalence ranged from 0% to 36% [11]. In another study, the prevalence rate of Cyclospora in 1088 stool samples from 544 symptomatic HIV positive cases was 2.2%, and no parasites were observed in asymptomatic cases [50]. Data accumulated in another systematic review of 14 sub-Saharan countries revealed an overall prevalence of C. cayetanensis of 18% [62].
It is important to note that the severity of disease caused by C. cayetanensis infection depends mainly on the host’s immune system. It is more severe in immunocompromised people, particularly PLWHA. A study carried out by Li et al. (2020) showed that the prevalence of C. cayetanensis was 7.38% (95% CI, 6.55–8.20%) in immunocompromised patients with diarrhea and 4.91% (95% CI, 4.35–5.47) in immunocompromised individuals without diarrhea. As a result, the reported prevalence of C. cayetanensis in this study was higher in people with diarrhea [63].
In our study, we showed that the highest and lowest prevalence rate among PLWHA was in North America and Asia, respectively. Cyclosporiasis is described in many countries, but it is most common in tropical and subtropical areas. It seems that the prevalence of this parasite is higher in underdeveloped and developing countries, and the effect of rainfall and weather on the prevalence of this parasite has already been shown [64]. We performed a meta-regression ratio for HIV and showed that the chances of contracting C. cayetanensis were 4.36 (95% CI, 2.00–9.48) in PLWHA.
We also found a significant relationship between C. cayetanensis infections and HIV patients (p < 0.05). Therefore, HIV infection is a risk factor for contracting this parasite. Immunodeficiency, especially HIV, and low CD4 counts are acknowledged important risk factors [65]. We also performed a ratio of patients’ CD4 counts <200 cells/mL and showed that these people had a 4.07 (95% CI, 1.37–12.12) chance of developing C. cayetanensis and that there was a significant relationship between CD4 counts and parasite infection (p < 0.05). HIV during its acute phase has been shown to cause a rapid decrease in CD4 cells in the lymphoid tissues of the gastrointestinal tract in the small and large intestine. Immune cells play an important role in repairing and maintaining the epithelial junction of the intestinal mucosa, and their discharge leads to impairment [66]. These cells integrate the mucosa of the intestinal wall, which in turn increases the transfer of microbes from the lumen into the lamina propria [67]. The immunity of those infected with HIV may be somewhat increased by HAART. Therefore, we also examined the relationship between C. cayetanensis infection and HAART. Our study showed that HAART significantly reduced the risk of C. cayetanensis infection. However, due to the limited data available, we could not find a significant relationship between them (p > 0.05). We continued to examine gender in the infection, but also owing to the lack of data, we could not see a significant difference between men and women (p > 0.05).
In general, our meta-analysis had several limitations. In most articles, there was not enough information about patients, so it was a limitation that we may missed some eligible data. Most of the studies except four [7,19,20,21] used direct methods of stool detection and staining. Diagnosis staining techniques included modified Ziehl–Neelsen (acid-fast), Safranin, Auramine, Rhodamine, Kinyoun, Giemsa, and Trichrome. The sensitivity of detection varies markedly between these techniques, depending on the protocol used and whether the oocysts are positively stained or not. Fluorescence-based microscopy provides an alternative means of detection. Nucleic acid-based methods provide an enhanced diagnostic and analytical performance, allowing for the specific and genotypic detection and identification of C. cayetanensis. Improved specificity and sensitivity were made possible largely through the use of PCR [68,69]. While microscopic diagnosis for this parasite is unreliable, the growing use of molecular methods may help to overcome some of the current diagnosis and treatment flaws. Due to the high sensitivity and accuracy of molecular methods, their use leads to more reliable results. By consequence, the gathering of these data may contribute to further reports and to the research and development for improved therapeutics.

5. Conclusions

In conclusion, the high prevalence of C. cayetanensis among PLWHA observed in this review emphasizes the need to implement screening and prophylaxis tailored to the local context for PLWHA. Data demonstrate that HIV-seropositive patients with diarrhea, CD4 cell count <200 cells/mL, and no antiviral treatment have higher prevalence of C. cayetanensis infection than other groups. These patients should receive early treatment for the non-specific symptoms caused by various parasitic diseases. Importantly, over the long interval between the time of infection and the onset of symptoms, physicians should treat the early symptoms of C. cayetanensis, such as diarrhea, in immunocompromised patients.

Author Contributions

Contributed to the design of the study, E.A., S.R., A.B., A.S.P. and M.d.L.P.; conducted the systematic review of the literature and extracted data, S.R., A.S.P., M.T.R. and S.A.H.; analyzed data and contributed to the interpretation of data, E.A., A.S.P., A.B., M.T.R., S.A.H., S.M.R.O. and M.d.L.P.; drafted the first version of the manuscript, S.R., A.S.P., S.A.H., A.B. and M.T.R.; revised the manuscript, E.A., M.d.L.P. and S.M.R.O. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by Infectious and Tropical Diseases Research Center, Tabriz University of Medical Sciences, Tabriz, Iran (Grant No. 67748), Project CICECO-Aveiro Institute of Materials, UIDB/50011/2020, UIDP/50011/2020, and LA/P/0006/2020, financed by national funds through the FCT/MEC (PIDDAC).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Viruses 14 01279 g001 550
Figure 1. Search strategy and study selection process indicating numbers of studies excluded or included using PRISMA flow diagram.
Figure 1. Search strategy and study selection process indicating numbers of studies excluded or included using PRISMA flow diagram.
Viruses 14 01279 g001
Viruses 14 01279 g002 550
Figure 2. Pooled prevalence of C. cayetanensis in HIV-infected patients in different continents.
Figure 2. Pooled prevalence of C. cayetanensis in HIV-infected patients in different continents.
Viruses 14 01279 g002
Viruses 14 01279 g003 550
Figure 3. Random-effects meta-analysis of C. cayetanensis infection in people living with HIV and/or AIDS (PLWHA).
Figure 3. Random-effects meta-analysis of C. cayetanensis infection in people living with HIV and/or AIDS (PLWHA).
Viruses 14 01279 g003
Viruses 14 01279 g004 550
Figure 4. Bias assessment plot displaying the prevalence estimate of prevalence of C. cayetanensis infection in people living with HIV and/or AIDS.
Figure 4. Bias assessment plot displaying the prevalence estimate of prevalence of C. cayetanensis infection in people living with HIV and/or AIDS.
Viruses 14 01279 g004
Table
Table 1. Assessment of risk of bias and quality in included studies.
Table 1. Assessment of risk of bias and quality in included studies.
NOFirst AuthorQ1Q2Q3Q4Q5Q6Q7Q8Q9Score
1J.W. Pape Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i003 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i0014
2J. Sifuentes Viruses 14 01279 i003 Viruses 14 01279 i003 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i003 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0014
3S. Manatsathit Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i003 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i0015
4Y. Germani Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i0016
5J.F. Lindo Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i003 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i0014
6J.P. Cegielski Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0016
7A. Escobedo Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i003 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0015
8T. Gumbo Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0017
9A. Mukhopadhya Viruses 14 01279 i001 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0015
10L. Chacin-Bonilla Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i0017
11R.A. Pratdesaba Viruses 14 01279 i001 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i0014
12S.S. Kumar Viruses 14 01279 i001 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i003 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i0014
13K. Mohandas Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i003 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0016
14K.-X. Wang Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i0016
15V. Capó de Paz Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0016
16L. Chacin-Bonilla Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0017
17C. Sarfati Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0017
18M.L. Becker Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0016
19R.G. Kaminsky Viruses 14 01279 i001 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0015
20S. Gupta Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0016
21C.P. Raccurt Viruses 14 01279 i001 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0016
22L. Tuli Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0029
23S. Kulkarni Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0016
24A. Kurniawan Viruses 14 01279 i002 Viruses 14 01279 i003 Viruses 14 01279 i003 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i0015
25W. Saksirisampant Viruses 14 01279 i001 Viruses 14 01279 i001 Viruses 14 01279 i003 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0015
26P. Viriyavejakul Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0016
27S. Babatunde Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0017
28I. Asma Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0029
29M. Agholi Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0017
30M.K. Mathur Viruses 14 01279 i001 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0015
31Z. Rivero-Rodríguez Viruses 14 01279 i001 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0015
32B.R. Tiwari Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0029
33N.H. Ahmed Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0029
34D.S. Nsagha Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0017
35M. Agholi Viruses 14 01279 i003 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0015
36S. Shah Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0028
37C.R. Swathirajan Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0016
38H.K. Uysal Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0016
39G. Alemu Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i001 Viruses 14 01279 i0016
40Y.K. Opoku Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0028
41O. Zorbozan Viruses 14 01279 i001 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0015
42H. Masoumi-Asl Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0017
43E.G. Rodríguez-Pérez Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i003 Viruses 14 01279 i003 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0015
44E.O. Udeh Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0028
45M.A.A.S. Namaji Viruses 14 01279 i001 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i001 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i002 Viruses 14 01279 i0015
Viruses 14 01279 i002 YES. Viruses 14 01279 i003 No. Viruses 14 01279 i001 Unclear/Not applicable.
Table
Table 2. Included studies of C. cayetanensis in people with HIV.
Table 2. Included studies of C. cayetanensis in people with HIV.
NOFirst AuthorYearCountryStudy DesignNo. of Participants/Positive PatientsMean AgeDiagnostic MethodPatients with DiarrheaPatients with CD4 <200Ref.
1J.W. Pape1994HaitiCohort450/4324Modified Kinyoun acid-fast450NR[22]
2J. Sifuentes1995Mexico CityCross-sectional235/740.5Modified acid-fast235NR[23]
3S. Manatsathit1996ThailandProspective study45/135Modified acid-fast4545[24]
4Y. Germani1998Central AfricanCase-control171/5NRModified trichrome171171[25]
5J.F. Lindo1998HondurasCross-sectional52/133.8Modified Kinyoun acid-fast16NR[26]
6J.P. Cegielski1999TanzaniaCase-control124/1NRKinyoun and auramine rhodamine124NR[27]
7A. Escobedo1999CubaCase-control67/227.9Modified Ziehl–NeelsenNRNR[28]
8T. Gumbo1999ZimbabweProspective study88/033Modified acid-fast88NR[29]
9A. Mukhopadhya1999IndiaCross-sectional111/5NRSafranine-Methylene blue and auramine61NR[30]
10L. Chacin-Bonilla2001VenezuelaRetrospective study71/733.5Modified Ziehl–Neelsen71NR[31]
11R.A. Pratdesaba2001GuatemalaCross-sectional157/632Modified acid-fastNRNR[32]
12S.S. Kumar2002IndiaCase-control152/140Modified Kinyoun acid- fast and Safranin Methylene blue102NR[33]
13K. Mohandas2002Northern IndiaCross-sectional120/4NRZiehl–Neelsen26NR[34]
14K.-X. Wang2002ChinaCase-control32/3NRAuramine phenol stain and modified acid-fast32NR[35]
15V. Capó de Paz2003CubaCross-sectional170/6NRZiehl–Neelsen170NR[36]
16L. Chacin-Bonilla2006VenezuelaCase-control74/637.3 ± 5.6Modified Ziehl–Neelsen74NR[37]
17C. Sarfati2006CameroonCross-sectional154/036Modified Ziehl–Neelsen46NR[38]
18M.L. Becker2007IndiaCase-control153/032.7 ± 8Acid-fast trichrome153NR[39]
19R.G. Kaminsky2007HondurasCross-sectional56/232.3Acid-fast trichrome18NR[40]
20S. Gupta2008IndiaCross-sectional113/133.2 ± 9.72 Modified acid-fast34NR[41]
21C.P. Raccurt2008HaitiCross-sectional67/27NRWeber modified trichrome67NR[42]
22L. Tuli2008IndiaCase-control366/8835.5Modified acid-fast and modified safranin366236[43]
23S. Kulkarni2009IndiaCross-sectional137/1M: 34.6 ± 7.51
F: 33.2 ± 9.95		Modified acid-fast13765[44]
24A. Kurniawan2009IndonesiaCross-sectional318/12NRModified acid-fastNRNR[45]
25W. Saksirisampant2009ThailandCross-sectional90/139.5Modified Ziehl–Neelsen71NR[46]
26P. Viriyavejakul2009ThailandCross-sectional64/3NRZiehl–Neelsen64NR[47]
27S. Babatunde2010NigeriaCross-sectional90/1635Modified Ziehl–Neelsen9026[48]
28I. Asma2011MalaysiaCross-sectional346/1721.5Modified Ziehl–Neelsen30189[49]
29M. Agholi2013IranCross-sectional356/137.18Acid-fast trichrome stain, nested PCR103188[19]
30M.K. Mathur2013IndiaRetrospective study544/1242.5Modified Ziehl–Neelsen400NR[50]
31Z. Rivero-Rodríguez2013VenezuelaCross-sectional56/235 ± 11.95Modified Kinyoun acid-fast48NR[51]
32B.R. Tiwari2013NepalCross-sectional745/1430Modified acid-fast248327[52]
33N.H. Ahmed2015IndiaCohort142/3NRModified Ziehl–Neelsen’s cold staining142NR[53]
34D.S. Nsagha2015CameroonCross-sectional300/1140Modified Ziehl–Neelsen11876[54]
35M. Agholi2016IranCross-sectional387/2NRModified acid-fast or acid-fast trichrome and semi-nested PCR387NR[7]
36S. Shah2016IndiaCross-sectional45/234.5Modified Ziehl–Neelsen2722[55]
37C.R. Swathirajan2017South IndiaCross-sectional829/2M: 38
F: 33.5		Modified acid-fast829NR[56]
38H.K. Uysal2017TurkeyCross-sectional115/341.5Ziehl–Neelsen and Kinyoun acid-fast, molecular methodsNR11[20]
39G. Alemu2018EthiopiaCross-sectional220/13NRModified Ziehl–Neelsen2143[57]
40Y.K. Opoku2018GhanaCross-sectional50/14NRZiehl–Neelsen50NR[8]
41O. Zorbozan2018TurkeyProspective study65/241.9 ± 12.4Modified acid-fast, Giemsa, Kinyoun65NR[58]
42H. Masoumi-Asl2019IranCross-sectional102/1NRAcid-fast and nested PCRNR9[21]
43E.G. Rodríguez-Pérez2019MexicoProspective study29/037Modified Ziehl–Neelsen, Giemsa and acid-fast trichromeNRNR[59]
44E.O. Udeh2019NigeriaCase-control891/9NRZiehl–NeelsenNR3[60]
45M. Namaji2020IndiaCross-sectional361/7NRModified acid-fast361NR[61]
Table
Table 3. Risk factors associated with C. cayetanensis infection in HIV patients.
Table 3. Risk factors associated with C. cayetanensis infection in HIV patients.
Risk FactorsNo. of StudiesCategoriesOR (95% CI)p-ValueI2 (Inconsistency) %Cochran Qp-Value
Sex3Male
Female		1.72 (0.79–3.73)p = 0.164702.06p = 0.7244
Diarrhea8Yes
No		3.23 (1.38–7.54)p = 0.006604.81p = 0.5675
CD410<200 cells/mL
>200 cells/mL		4.07 (1.37–12.12)p = 0.011574.535.24p < 0.0001
HAART3No
Yes		2.07 (0.29–14.81)p = 0.4668-1.57p = 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

AMA Style

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 Style

Ramezanzadeh, 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

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