|Year : 2021 | Volume
| Issue : 3 | Page : 99-112
Prevalence of cryptosporidiosis in animals in Iran: A systematic review and metaanalysis
Mohammad Jokar1, Mohammad Hasan Rabiee2, Saied Bokaie2, Vahid Rahmanian3, Paria Dehesh4, Hamideh Hasannejad2, Kiavash Hushmandi2, Hadi Keshipour2
1 Faculty of Veterinary Medicine, Karaj Branch, Islamic Azad University, Karaj, Iran
2 Divisions of Epidemiology, Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, University of Tehran, Iran
3 Zoonoses Research Center, Jahrom University of Medical Sciences, Jahrom, Iran
4 Department of Epidemiology, School of Public Health, Iran University of Medical Sciences, Tehran, Iran
|Date of Submission||24-Nov-2020|
|Date of Decision||14-Jan-2021|
|Date of Acceptance||15-Jan-2021|
|Date of Web Publication||02-Feb-2021|
Divisions of Epidemiology, Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, University of Tehran
Source of Support: None, Conflict of Interest: None
Objective: To review the prevalence of cryptosporidiosis among animal population of Iran.
Methods: Data were systematically gathered from 1 January 2000 to 1 January 2020 in the Islamic Republic of Iran from the following electronic databases: PubMed, Springer, Google Scholar, Science Direct, Scopus, Web of Science, Magiran, and Scientific Information Database (SID). According to the preferred reporting items for systematic reviews and meta-analyses (PRISMA) and inclusion criteria, 88 eligible studies were obtained.
Results: The pooled prevalence of cryptosporidiosis using random and fixed effects model according to heterogeneity among animals was as follows: rodents 18.8% (95% CI 12.6%-25.0%), camels 17.1% (95% CI 8.6%-25.7%), cattle 16.8% (95% CI 13.4%-20.1%), goats 14.1% (95% CI 5.2%-23.0%), horses 12.2% (95% CI 8.3%- 16.2%), birds 10.5% (95% CI 7.6%-13.4%), sheep 9.9% (95% CI 2.4%-4.9%), cats 8.8% (95% CI 4.8%-12.8%) and dogs 3.7% (95% CI 7.0%-12.8%).
Conclusions: Cryptosporidiosis has been reported and present in a wide range of animals in Iran over the years and has a high prevalence in most of these species.
Keywords: Cryptosporidiosis; Animals; Prevalence; Iran
|How to cite this article:|
Jokar M, Rabiee MH, Bokaie S, Rahmanian V, Dehesh P, Hasannejad H, Hushmandi K, Keshipour H. Prevalence of cryptosporidiosis in animals in Iran: A systematic review and metaanalysis. Asian Pac J Trop Med 2021;14:99-112
|How to cite this URL:|
Jokar M, Rabiee MH, Bokaie S, Rahmanian V, Dehesh P, Hasannejad H, Hushmandi K, Keshipour H. Prevalence of cryptosporidiosis in animals in Iran: A systematic review and metaanalysis. Asian Pac J Trop Med [serial online] 2021 [cited 2021 May 15];14:99-112. Available from: https://www.apjtm.org/text.asp?2021/14/3/99/307532
| 1. Introduction|| |
Cryptosporidium is one of the zoonotic parasites. It is a genus in the family Cryptosporiidae, suborder Eimeriorina, order Eucoccidiorida, subclass Coccidiasina, class Sporozoasida and phylum Apocomplexa. The protozoan, for first time identified by Tyzzer (1907) in mice and so far nearly 40 valid species and more than 50 genotypes of it has been recognized. This parasite infects a wide range of vertebrates including mammals, birds, amphibians, reptiles and aquatic animals and affects the epithelial cells of their gastrointestinal tract to causes a disease with a wide range of form, from asymptomatic to mild and severe gastrointestinal symptoms,.
Cryptosporidiosis is one of the major causes of diarrheal death in children less than five years old and young animals, especially neonatal of ruminants,. Furthermore, this infection is life-threatening for immunosuppressed patient, notably HIV-infected people that recent systematic review has shown a high prevalence of cryptosporidiosis in them,. Various clinical signs of cryptosporidiosis are reported in mammals and birds such as diarrhea, anorexia, lethargy, lower pigmentation, apathy and depression, growth retardation and finally death,.
Cryptosporidiosis in companion animals is asymptomatic but infrequently with concurrent infections, different signs have been reported in horses, cats and dogs,. The important economic losses in ruminants farms are caused by acute diarrhea,. This infection frequently occurs in reptiles but may be life-threatening for them.
Several concerns exist in the global control of cryptosporidiosis: firstly, different transmission routes such as person-to-person, human-animal, foodborne and waterborne transmission; secondly, inefficiency of water disinfectants against Cryptosporidium oocyte; thirdly, the absence of a vaccine and effective treatment,.
The epidemiological aspects of cryptosporidiosis among animals’ populations can be useful for setting control plans. To the best of our knowledge, till now, there is no available knowledge about the pooled prevalence of Cryptosporidium infection in animals’ populations of Iran. Accordingly, we conducted a systematic review and meta-analysis to establish the overall prevalence of cryptosporidiosis in animals in Iran.
| 2. Materials and methods|| |
This study was designed as suggested via the preferred reporting items for systematic reviews and meta-analyses (PRISMA).
2.1. Bibliographic search strategy
The relevant studies have been identified from 1 January 2000 to 1 January 2020 from six English sources i.e. PubMed, Springer, Google Scholar, Science Direct, Scopus, and Web of Science and two Persian databases namely Magiran, and Scientific Information Database (SID). The search was implemented using the MeSH terms as follows: “Cryptosporidium” or “cryptosporidiosis” or “intestinal parasite” and “Iran” in combination and in both Persian (Farsi) and English. In addition, the datasets option of “related articles” and the reference of the studies was checked to prevent missing data. The selection process of studies is in view in the PRISMA flowchart as shown in [Figure 1].
|Figure 1: PRISMA flowchart presenting the selection of articles analyzed in this systematic review and meta-analysis.|
Click here to view
2.2. Inclusion and exclusion criteria
The title and abstract of studies related to animal cryptosporidiosis in Iran were screened. After eliminating duplicates, the full text of papers was reviewed by two reviewers independently for assessing the quality of the articles. Differences of opinion between the specialists were resolved by a third person independently and consensus.
Inclusion criteria for our study were: (1) studies conducted on animal's population of Iran; (2) studies that reported prevalence of cryptosporidiosis; (3) studies which diagnosed cryptosporidiosis based on microscopic method.
Exclusion criteria included the following: (1) any studies whose type was non-cross-sectional (experimentally, case report and etc.); (2) studies not performed on Iran; (3) studies not performed on animal populations; (4) studies not reported prevalence of cryptosporidiosis; (5) studies not detected Cryptosporidium based on microscopic methods; (6) studies in which the method of detecting Cryptosporidium was ambiguous.
2.3. Data collection
An Excel data extraction form was used to collect the following data from eligible studies: first author, time of publication, time of study, place of study, animal species, diagnostic tests, sample size, total Cryptosporidium-positive number, prevalence, age group, gender, type of habitat or farming system, absence or presence of diarrheal sign and season [Table 1].
2.4. Statistical analysis
The pooled prevalence and 95% confidence intervals (CI) were estimated using random and fixed-effects models. The heterogeneity was expected in advance, and statistical methods, Cochran's Q test and I2 index were used to assess the heterogeneity among the studies. if I2 index > 50% and Cochran's Q test P-value < 0.1, we would choose the random effect model for estimation. Proportions of individual studies, overall prevalence and the heterogeneity among studies were presented by forest plots.
The publication bias of studies was assessed by Egger's test. To visualize the cattle and dogs cryptosporidiosis in Iran, we used the Arc GIS 10.3 software (https://www.arcgis.com) to map the distribution of prevalence in different provinces. The meta-analysis was performed with the trial version of StatDirect statistical software available from public domain i.e. http://statdirects.com.
| 3. Results|| |
3.1. Search results and eligibility studies
In this study, totally 1 586 articles were found by searching the entire databases; by systematic review and meta-analysis by considering the inclusion criteria. Among them, 548 articles were removed due to duplication and 854 articles were removed due to non-compliance with inclusion and exclusion criteria in caption and abstract. Also, 96 articles were removed due to non-compliance with inclusion and exclusion criteria in full text. Eventually 88 studies have met the evaluation criteria of this study [Figure 1].
3.2. Characteristics of the eligible studies
Among the 88 eligible studies, 22 were published before 2010 and others published after 2010. Among the studies, 78 studies determined prevalence only in one species of animal, while 10 studies determined the prevalence in more than one species. In the other words, studies determined prevalence are as follows: 30 among cattle, 19 among dogs, 16 among birds 10 among rodent, 7 among sheep, 6 among camels, 5 among horses, 3 among cat, 3 among goats, 2 among buffalos, 1 among fish and 1 among mules. Also, 86 studies reported prevalence only in one province while 2 studies reported prevalence in more than one province [Table 1].
3.3. Prevalence of cryptosporidiosis
3.3.1. Prevalence of cryptosporidiosis in cattle
A total number of 8 684 cattle were examined for cryptosporidiosis in different geographical locations in Iran and 1 316 cases were detected positive using microscopic method presented [Table 2]. Overall, the pooled prevalence of cryptosporidiosis using random-effects meta-analysis among cattle was estimated at 16.8% (95% CI 13.4%-20.1%) [Table 2] and [Figure 2]. There was a high degree of heterogeneity in the prevalence estimates between different studies. It was observed Q statistic=958.45 (df=29), P<0.01, and I2=97.0% [Table 2]. The pooled prevalence of cryptosporidiosis in cattle was higher in summer, diarrheal patients, bulls and cattle less than 1 year old but none of them had a significant difference [Table 3]. In addition, a schematic map of cryptosporidiosis distribution in cattle was made based on studies conducted in the provinces of Iran [Figure 3].
|Figure 2: Forest plots of prevalence of cryptosporidiosis among cattle (A), dogs (C), and cats (E) in Iran (first author, year) with funnel plot for visualization of publication bias in studies of cattle (B), dogs (D) and cats (F).|
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|Figure 3: Prevalence of cryptosporidiosis among cattle (A) and dogs (B) in different provinces of Iran.|
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|Table 3: Demographic factors associated with positivity of Cryptosporidium in the Iranian animal population.|
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3.3.2. Prevalence of cryptosporidiosis in dogs
A total number of 4 107 dogs were examined for cryptosporidiosis in different geographical locations in Iran and 183 cases were detected positive using microscopic method as presented [Table 2]. Overall, the pooled prevalence of cryptosporidiosis using random-effects meta-analysis among dogs was estimated at 3.7% (95% CI 2.4%-4.9%) [Table 2] and [Figure 2]. There was a high degree of heterogeneity in the prevalence estimates between different studies was observed Q statistic=141.01 (df=19), P<0.01, and I2=86.5% [Table 2]. The pooled prevalence of cryptosporidiosis in dogs was higher in fall, stray dogs, female and dog's upper than 1 year old but none of them had a significant difference [Table 3]. In addition, a schematic map of cryptosporidiosis distribution in dogs was made based on studies conducted in the provinces of Iran [Figure 3].
3.3.3. Prevalence of cryptosporidiosis in cats
A total number of 187 cats were examined for cryptosporidiosis in different geographical locations in Iran and 19 cases were detected positive using microscopic method as presented [Table 2]. The results show that there are 3 studies estimate the prevalence of Cryptosporidium in 187 stray cats and the pooled prevalence was 8.8% (95% CI 4.8%-12.8%) using the fixed-effect model [Table 2] and [Figure 2]. There was an intermediate degree of heterogeneity in the prevalence estimates between different studies. It was observed Q statistic=3.39 (df=2), P=0.184, and I2=41.0% [Table 2].
3.3.4. Prevalence of cryptosporidiosis in sheep
A total number of 3 901 sheep were examined for cryptosporidiosis in different geographical locations in Iran and 395 cases were detected positive using microscopic method as presented [Table 2]. Overall, the pooled prevalence of cryptosporidiosis using random-effects meta-analysis among sheep was estimated at 9.9% (95% CI 7.0%-12.8%) [Table 2] and [Figure 4]. There was a high degree of heterogeneity in the prevalence estimates between different studies. It was observed Q statistic=114.90 (df=11), P<0.01, and I2=90.4% [Table 2]. The pooled prevalence of cryptosporidiosis in sheep was higher in male and sheep under 1 year old but none of them had a significant difference [Table 3].
|Figure 4: Forest plots of prevalence of cryptosporidiosis among sheep (A), goats (C), and birds (E) in Iran (first author, year) with funnel plot for visualization of publication bias in studies of sheep (B), goats (D) and birds (F).|
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3.3.5. Prevalence of cryptosporidiosis in goats
A total number of 1 030 goats were examined for cryptosporidiosis in different geographical locations in Iran and 147 cases were detected positive using microscopic method as presented [Table 2]. The results show that there are 3 studies estimate the prevalence of Cryptosporidium in goats and the pooled prevalence using the random effects model of 14.1% (95% CI 5.2%-23.0%) [Table 2] and [Figure 4]. There was a high degree of heterogeneity in the prevalence estimates between different studies. It was observed Q statistic=37.87 (df=2), P<0.01, and I2=94.7% [Table 2].
3.3.6. Prevalence of cryptosporidiosis in birds
A total number of 3 352 birds were examined for cryptosporidiosis in different geographical locations in Iran and 307 cases were detected positive using microscopic method as presented [Table 2]. Overall, the pooled prevalence of cryptosporidiosis, using random- effects meta-analysis among birds was estimated at 10.5% (95% CI 7.6%-13.4%) [Table 2] and [Figure 4]. There was a high degree of heterogeneity in the prevalence estimates between different studies. It was observed Q statistic=165.28 (df=15), P<0.01, and I2=90.9% [Table 2]. The pooled prevalence of cryptosporidiosis in birds was higher in commercial farming system but there was no significant difference [Table 3].
3.3.7. Prevalence of cryptosporidiosis in horses
A total number of 636 horses were examined for cryptosporidiosis in different geographical locations in Iran and 85 cases were detected positive using Microscopic method as presented [Table 2]. Overall, the pooled prevalence of cryptosporidiosis using random-effects meta-analysis among horses was estimated at 12.2% (95% CI 8.3%-16.2%) [Table 2] and [Figure 5]. There was an intermediate degree of heterogeneity in the prevalence estimates between different studies. It was observed Q statistic=9.49 (df=4), P=0.05, and I2=57.9% [Table 2]. The pooled prevalence of cryptosporidiosis in horses was higher in female horses but there was no significant difference [Table 3].
|Figure 5: Forest plots of prevalence of cryptosporidiosis among horses (A), rodents (C), and camels (E) in Iran (first author, year) with funnel plot for visualization of publication bias in studies of horses (B), rodents (D) and camels (F).|
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3.3.8. Prevalence of cryptosporidiosis in rodents
A total number of 976 rodents were examined for cryptosporidiosis in different geographical locations in Iran and 133 cases were detected positive using microscopic method as presented [Table 2]. Overall, the pooled prevalence of cryptosporidiosis using random-effects meta-analysis among rodents was estimated at 18.8% (95% CI 12.6%-25.0%) [Table 2] and [Figure 5]. There was a high degree of heterogeneity in the prevalence estimates between different studies. It was observed Q statistic=384.85 (df=9), P<0.01, and I2=97.7% [Table 2].
3.3.9. Prevalence of cryptosporidiosis in camel
A total number of 1 029 camels were examined for cryptosporidiosis in different geographical locations in Iran and 187 cases were detected positive using microscopic method as presented [Table 2]. Overall, the pooled prevalence of cryptosporidiosis using random-effects meta-analysis among camels was estimated at 17.1% (95% CI 8.6%-25.7%) [Table 2] and [Figure 5]. There was a high degree of heterogeneity in the prevalence estimates between different studies. It was observed Q statistic=87.27 (df=5), P<0.01, and I2=94.3% [Table 2]. The pooled prevalence of cryptosporidiosis in camels was higher in female and camels upper than 5 years old but none of them had a significant difference [Table 3].
3.3.10. Prevalence of cryptosporidiosis in other animals
Two studies reported the prevalence in buffalo was 45% and 2% respectively. One study reported the prevalence in mules was 12.5% and one study reported prevalence in fish was 17% [Table 2].
3.4. Publication bias
Egger tests were applied to check the presence of publication bias. The Egger's test in cattle, sheep, goats, dogs, birds, and rodents, indicated a significant publication bias of studies [Table 2].
| 4. Discussion|| |
In this systematic review and meta-analysis, we reviewed the prevalence of cryptosporidiosis among all animals’ species in Iran. To detect cryptosporidiosis, there are microscopic, serological, and molecular methods, each with its own characteristics. However, acid-fast staining of fecal smear for displaying the Cryptosporidium oocytes is one practical and rapid method, and in low-income countries, this method is commonly used because of inexpensive, simple and having a high positive predictive value for Cryptosporidium,. Therefore, in this meta-analysis, the pooled prevalence of cryptosporidiosis was estimated among the studies that had reported the prevalence of this infection in Iran using microscopic methods.
In this study, we indicated that the pooled prevalence among animal of Iran was between 3.7% to 18.8% and the pooled prevalence respectively was high to low as follows: rodent, camel, cattle, goats, horse, birds, sheep, cat and dog. Notably we prioritized it regardless of study of buffalo, fish and mule which had less than two studies. This different prevalence among animal can be due to different susceptibility of animals to the Cryptosporidium and also different raising and living areas. Anyway, In general, this result shows that the disease has been reported in a wide range of animals in Iran for many years and it is necessary to pay more attention to it among animals because of its economic and public health importance.
As we showed, rodents have the highest pooled prevalence of cryptosporidiosis compared to other animals of Iran. Indeed, the pooled prevalence of cryptosporidiosis in rodents using the microscopic detection method was estimated at 18.8% in the present study. A global meta-analysis estimated the pooled prevalence of cryptosporidiosis using the microscopic method was 14% in rodents. The infection of different rodent species by Cryptosporidium spp. has been reported in different parts of the world, as well as the transmission of this pathogen by rodents to humans has been proven,. Besides, in recent decades, the rapid development of industry and agriculture, climate change has increased the probability of humans-rodents contact. Therefore, considering that the estimated pooled prevalence of rodent's cryptosporidiosis was high in Iran and given presence of various species of rodent in different parts of the country, it is essential to control rodent's population and accessibility of them to water and food supply for reaching one health condition.
In addition to rodents, this study indicated that prevalence of cryptosporidiosis among other mentioned animals was remarkable. For instance, the prevalence among camels, cattle, goats, horses, birds and sheep was as follows: 17.1%, 16.8%, 14.1%, 12.2%, 10.5% and 9.9%. Although cryptosporidiosis is important in all of these animals, it is more important in cattle, and most studies published on animal cryptosporidiosis in different countries have been conducted on bovine cryptosporidiosis. So far, different meta-analyses have determined pooled prevalence of cryptosporidiosis among cattle in different regions. For instance, a meta-analysis study in China estimated the pooled prevalence of cryptosporidiosis in cattle till 2019, regardless of the type of detection method, was 17%, and with the microscopic method being 16.5%. Also, other meta-analyses conducted in Nigeria and Colombia estimated the pooled prevalence of this infection in cattle, regardless of the diagnostic method, was 26.1% and 21%, respectively,. Although the disease rarely causes death in cattle and calves, it can cause great economic losses to the industry due to diarrhea, dehydration and weight loss. Furthermore, the bovine population is one of the most important animal reservoirs in disease transmission to humans by shedding oocytes and consequently contaminating of water and food supply. Therefore, given high pooled prevalence among cattle in Iran, it is important to control of the disease in cattle population to prevent Cryptosporidium transmission to other hosts and especially human and also to reduce the economic losses due to its occurrence.
The lowest pooled prevalence of cryptosporidiosis among animals of Iran was in cats and dogs population with 8.8% and 3.7% respectively. A global meta-analysis in the dog's population estimated the pooled prevalence of cryptosporidiosis (using the microscopic method) was 8% and the range of pooled prevalence was from 0% to 13% in different parts of the world. Furthermore, the meta-analysis study in Colombia estimated the pooled prevalence of Cryptosporidium infection in dogs and cats was 17.4% and 13%, respectively. The much lower prevalence of this disease in dogs in this study, as well as to some extent in similar studies, could be due to the fact that the majority of dogs studied are domestic dogs and because of the greater attention of their owners, the possibility of infection in them is less. However, various studies have proven the role of dogs and cats in transmitting the disease to humans. Besides, dogs and cats are known as the most important human friends and keeping dogs and cats at home has increased in the last decade in Iran. Accordingly, observing hygienic practices for veterinarians and providing instruction for animal lovers before preparing dogs and cats can help control this infectious zoonotic aspect.
The strengths of this study include the large total sample size, the comprehensive literature search in eight international and Iranian databases, and vast population study (all animal species). However, this study has some limitations and the results presented here should be interpreted with regard to these limitations. Limitations include some reports with low sample size, high heterogeneity, and the possibility that our search strategy missed some studies.
In conclusion, the results of this systematic review and meta-analysis showed that cryptosporidiosis has been reported and present in a wide range of animals in Iran over the years and has a high prevalence in most of these species. Given that this disease causes economic and health damage, there is a need for health officials, veterinarians and livestock owners to try to improve the breeding environment and life of animals to prevent disease in them, not only to protect animal health and prevent economic losses in the case of farmed animals, but also to protect human health.
Conflict of interest statement
The authors declare that there are no conflicts of interest.
M.H.R, S.B and V.R participated in study design. M.J, P.D, H.H, K.H and H.K did literature mining and data acquisition. M.J and M.H.R drafted the manuscript. Review and editing of the manuscript were done by M.H.R, M.J, S.B and V.R. All authors approved the final draft for publication.
| References|| |
Nader JL, Mathers TC, Ward BJ, Pachebat JA, Swain MT, Robinson G, et al. Evolutionary genomics of anthroponosis in Cryptosporidium. Nat Microbiol
Tzipori S, Widmer G. A hundred-year retrospective on cryptosporidiosis. Trends Parasitol
Ryan U, Fayer R, Xiao L. Cryptosporidium
species in humans and animals: Current understanding and research needs. Parasitology
Khalil IA, Troeger C, Rao PC, Blacker BF, Brown A, Brewer TG, et al. Morbidity, mortality, and long-term consequences associated with diarrhoea from Cryptosporidium
infection in children younger than 5 years: A meta-analyses study. Lancet Glob Heal
Thomson S, Hamilton CA, Hope JC, Katzer F, Mabbott NA, Morrison LJ, et al. Bovine cryptosporidiosis: Impact, host-parasite interaction and control strategies. Vet Res
Marcos LA, Gotuzzo E. Intestinal protozoan infections in the immunocompromised host. Curr Opin Infect Dis
Wang ZD, Liu Q, Liu HH, Li S, Zhang L, Zhao YK, et al. Prevalence of Cryptosporidium
, microsporidia and Isospora
infection in HIV-infected people: A global systematic review and meta-analysis. Parasit Vectors
Alvarez-Pellitero P, Sitjà-Bobadilla A. Cryptosporidium molnari
n. sp. (Apicomplexa: Cryptosporidiidae) infecting two marine fish species, Sparus aurata
L. and Dicentrarchus labrax
L. Int J Parasitol
Santín M. Clinical and subclinical infections with Cryptosporidium
in animals. N Z Vet J
Thompson RCA, Olson ME, Zhu G, Enomoto S, Abrahamsen MS, Hijjawi NS. Cryptosporidium
and cryptosporidiosis. Adv Parasitol
77-158. doi: 10.1016/S0065-308X(05)59002-X.
De Graaf DC, Vanopdenbosch E, Ortega-Mora LM, Abbassi H, Peeters JE. A review of the importance of cryptosporidiosis in farm animals. Int J Parasitol
Deming C, Greiner E, Uhl EW. Prevalence of Cryptosporidium
infection and characteristics of oocyst shedding in a breeding colony of leopard geckos (Eublepharis macularius). J Zoo Wildl Med
Meinhardt PL, Casemore DP, Miller KB. Epidemiologic aspects of human cryptosporidiosis and the role of waterborne transmission. Epidemiol Rev
Ryan U, Zahedi A, Paparini A. Cryptosporidium
in humans and animals-a one health approach to prophylaxis. Parasite Immunol
Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. PLoS Med
(7): e1000100. doi: 10.1371/journal.pmed.1000100.
Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. Br Med J
DerSimonian R, Laird N. Meta-analysis in clinical trials revisited. Contemp Clin Trials
Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. Br Med J
Khanzadeh-Karvigh A, Yakhchali M, Hadian M. A comparative study on Cryptosporidium
infection in household and stray dogs in Urmia and Tabriz municipalities, Iran. Vet Res Biol Prod
Larki S, Alborzi A, Chegini R, Amiri R. A preliminary survey on gastrointestinal parasites of domestic ducks in Ahvaz, Southwest Iran. Iran J Parasitol
Lotfollahzadeh S, Ziaei Daroonkolai N, Zahraei Salehi T, Poorbakhsh SA, Mokhber Dezfouli MR, Afshari GR. A study on the presence of Escherichia coli
, coccidia spp. and Cryptosporidium
spp. in faecal samples of neonatal diarrhoeic calves in Ghaemshahr and Babol and antibiotic sensitivity of isolates. J Fac Vet Med Univ Tehran
Radfar MH, Fathi S, Asl EN, Dehaghi MM, Seghinsara HR. A survey of parasites of domestic pigeons (Columba livia domestica)
in South Khorasan, Iran. Vet Res
Azizi HR, Pourjafar M, Dabaghzadeh B, Rajabi H. A survey of prevalence of Cryptosporidium parvum
infection in less than 1 year old calves in Shahrekord dairy farms. Iran Vet J
Tavasouli M, Sodagar SM, Soltan AF. A survey on cryptosporidial infection in horse in Urmia area, Northwestern Iran. Iran J Vet Res
Keyvanloo Shahrestanakey R, Taghavi Razavizadeh A, Razmi GH. A survey on Cryptosporidium
spp. infection in lambs with and without clinical signs of diarrhea in Jovein area. Vet Clin Pathol (Vet J Tabriz)
Ghadrdan Mashhadi A, Hamidienjat H, Alizadehnia P. A survey on frequency of equine cryptosporidiosis in Ahvaz. Vet Clin Pathol (Vet J Tabriz)
Borji H, Khoshnegah J, Razmi G, Amini H, Shariatzadeh M. A survey on intestinal parasites of golden hamster (Mesocricetus auratus)
in the northeast of Iran. J Parasit Dis
Pirestani M, Sadraei J, Dalimi Asl AH. A survey on prevalence rate of cryptosporidial infection of farms in Shahriar county of Tehran and its hygienic importance in human. Vet J
Maleki SH, Nayebzadeh H. A survey on prevalence rate of cryptosporidiosis among diarrheic and healty cattle and calves in Khoram-abad, Iran. J Vet Res
Mohaghegh MA, Vafaei MR, Ghomashlooyan M, Azami M, Falahati M, Azadi Y, et al. A wide diversity of zoonotic intestinal parasites in domestic and stray dogs in rural areas of Kermanshah province, Iran. Trop Biomed
Mosallanejad B, Hamidinejat H, Avizeh R, Ghorbanpoor Najafabadi M, Razi Jalali MH. Antigenic detection of Cryptosporidium parvum
in urban and rural dogs in Ahvaz district, southwestern Iran. Iran J Vet Res
Radfar MH, Gowhari MA, Khalili M. Comparison of capture ELISA and modified Ziehl-Neelsen for detection of Cryptosporidium parvum
in feces of camel (Camelus dromedarius)
in Iran. Sci Parasitol
Mirzaei M, Fooladi M. Coproscopy survey of gastrointestinal parasites in owned dogs of Kerman city, Iran. Vet Ital
Ranjbar-Bahadori Sh, Sangsefidi H, Shemshadi B, Kashefinejad M. Cryptosporidiosis and its potential risk factors in children and calves in Babol, North of Iran. Trop Biomed
Fasihi Harandi M, Fotouhi Ardakani R. Cryptosporidium
infection of sheepand goats in Kerman: Epidemiologyand risk factor analysis. J Vet Res
Mirzai Y, Yakhchali M, Mardani K. Cryptosporidium parvum
and Cryptosporidium andersoni
infection in naturally infected cattle of northwest Iran. Vet Res Forum
Heidarnegadi SM, Mohebali M, Maraghi S, Babaei Z, Farnia S, Bairami A, et al. Cryptosporidium
spp. infection in human and domestic animals. Iran J Parasitol
Mirzaghavami M, Sadraei J, Forouzandeh M. Detection of Cryptosporidium
spp. in free ranging animals of Tehran, Iran. J Parasit Dis
Mirzaei M, Ramezanpour A. Diagnosis of Cryptosporidium
infection in companion dogs in Kerman city. J Vet Lab Res
Pestechian N, Rasouli A, Yoosefi H. Distribution of intestinal worms among stray dogs in Isfahan, Iran. J Isfahan Med Sch
Nourmohammadzadeh F, Davoodi Y, Jamali R, Nowrouzian I. Epidemiologicalstudyon cryptosporidiosis in newborn calves in eastern Azarbaijan province. J Vet Res
Mirzaei M. Epidemiological survey of Cryptosporidium
spp. in companion and stray dogs in Kerman, Iran. Vet Ital
Bahrami A, Doosti A, Nahravanian H, Noorian AM, Asbchin SA. Epidemiological survey of gastro-intestinal parasites in stray dogs and cats. Aust J Basic Appl Sci
Fotouhi Ardakani R, Fasihi Harandi M, Solayman Banai S, Kamyabi H, Atapour M, Sharifi I. Epidemiology of Cryptosporidium
infection of cattle in Kerman/Iran and molecular genotyping of some isolates. J Kerman Univ Med Sci
Behzadi MA, Razavi SM, Yazdanpoor H, Mirzaei A, Tamadon A, Gandomani MJ. Epidemiology of Cryptosporidium
infection in ostriches (Struthio camelus)
in Iran. Bulg J Vet Med
Rasuli S, Khodadadi A, Sadagiyani M, Moradpoor A, Salmanzadeh R. Equine Cryptosporidium
prevalence in border line villages of Urmia province. J Vet Clin Res
Badparva E, Ezatpour B, Azami M, Badparva M. First report of birds infection by intestinal parasites in Khorramabad, west Iran. J Parasit Dis
Haghbin Nazarpak H, Mousavi SA, Ranjbar Bahadori SH, Mohammadi Malayeri MR, Hoseini SM. Frequency of Cryptosporidium
infection in broiler breeding flock of Ghaemshahr. Vet Res (Garmsar Branch)
Tavassoli M, Iran U, Javadi S, Soltanalinejad F, Rosouli S, Etminanfar R. Gastrointestinal parasites of pet dogs in Urmia city. Vet J
Mohaghegh MA, Kalani H, Azami M, Falahati M, Heydarian P, Ghomashlooyan M. Gastrointestinal parasitic infection in laboratory rats: A challenge for researchers. Comp Clin Path
Nematollahi A, Jaberi S, Helan JA, Sheikhzadeh N. Histopathological study on parasites in freshwater ornamental fishes in Iran. J Parasit Dis
Arzamani K, Rouhani S, Mousazadeh-Mojarrad A, Sedeghi S, Rostami M, Raeghi S. Identification of zoonotic parasites isolated from stray dogs in Bojnurd county located in North-East of Iran. Nov Biomed
Ranjbar-Bahadori Sh, Toni S. Infection to Cryptosporidium
in diarrheic calves: A provincial study in southern Khorasan. J Vet Res
Hamedi H, Heydari M, Soleymani Ahmadi M. Intestinal and blood parasites of brown rats in Bandar Abbas. Hormozgan Med J
Gharagozlou MJ, Dezfoulian O, Rahbari S, Bokaie S, Jahanzad I, Razavi ANE. Intestinal cryptosporidiosis in Turkeys in Iran. J Vet Med Ser A Physiol Pathol Clin Med
Dalimi A, Mojarad S, Jamshidi SH. Intestinal parasites of pet dogs in Tehran and evaluation of knowledge of dog owners about zoonotic risk of parasites of dog. J Vet Res
Mahami Oskouei M, Fallah E, Ahmadi M, Safaiyan A, Bakhtiyari S, Naserifar R, et al. Molecular and parasitological study of Cryptosporidium
isolates from cattle in Ilam, west of Iran. Iran J Parasitol
Fallah E, Poor BM, Jamali R, Nahavandi KH, Asgharzadeh M. Molecular characterization of Cryptosporidium
isolates from cattle in a slaughterhouse in Tabriz, Northwestern Iran. J Biol Sci
Saki J, Asadpouri R. Molecular characterization of Cryptosporidium
species isolated from cattle in southwest of Iran. Jundishapur J Microbiol
(5). doi: 10.5812/jjm.59371.
Saki J, Foroutan-Rad M, Asadpouri R. Molecular characterization of Cryptosporidium
spp. in wild rodents of southwestern Iran using 18s
rRNA gene nested-PCR-RFLP and sequencing techniques. J Trop Med
6834206. doi: 10.1155/2016/6834206.
Hamidinejat H, Jalali MHR, Jafari RA, Nourmohammadi K. Molecular determination and genotyping of Cryptosporidium
spp. in fecal and respiratory samples of industrial poultry in Iran. Asian Pac J Trop Med
Jalas M, Tavalla M. Molecular diagnosis and genetic diversity of Cryptosporidium
spp. in exotic birds of southwest of Iran. Trop Biomed
Dalimi A, Tahvildar f, Kazemi B. Molecular identification of Cryptosporidium andersoni
in Shahriar calves. Vet J (Pajouhesh Sazandegi)
Mohammadi Ghalehbin B, Arzanlou M, Fallah E, Kazemi AH, Asgharzadeh M. Molecular identification of Cryptosporidium
sp. in the cattle stool samples in Ardabil city, Northwestern Iran. J Anim Vet Adv
Ranjbar R, Mirhendi H, Izadi M, Behrouz B, Mohammadi Manesh R. Molecular identification of Cryptosporidium
spp. in Iranian dogs using seminested PCR: A first report. Vector-Borne Zoonotic Dis
Tavalla M, Kord E, Abdizadeh R, Asgarian F. Molecular study of Cryptosporidium
spp. in dogs from southwest of Iran. Jundishapur J Microbiol
(4). doi: 10.5812/jjm.43412.
Mohebali M, Zarei Z, Khanaliha K, Kia EB, Motavalli-Haghi A, Davoodi J, et al. Natural intestinal protozoa in rodents (Rodentia: Gerbillinae, Murinae, Cricetinae) in northwestern Iran. Iran J Parasitol
Keshavarz A, Haghighi A, Athari A, Kazemi B, Abadi A, Mojarad EN. Prevalence and molecular characterization of bovine Cryptosporidium
in Qazvin province, Iran. Vet Parasitol
Asadpour M, Razmi G, Mohhammadi G, Naghibi A. Prevalence and molecular identification of Cryptosporidium
spp. in pre-weaned dairy calves in Mashhad area, Khorasan Razavi province, Iran. Iran J Parasitol
Ali H, Mohammad M, Saeid S. Prevalence of cryptosporidiosis in foals and humans to be in contact them in Tabriz Rea in Iran. Adv Environ Biol
Davoudi J, Shirazi SH, Mostofi S, Vahidi Madadlou S. Prevalence of cryptosporidiosis spp in children, calf and rat in Tabriz city. Vet Res (Garmsar Branch)
Borji H, Razmi G, Movassaghi AR, Naghibi AG, Maleki M. Prevalence of Cryptosporidium
infections in dromedary (Camelus dromedarius)
in abattoir of Mashhad, Iran. J Camel Pract Res
Razavi SM, Oryan A, Bahrami S, Mohammadalipour A, Gowhari M. Prevalence of Cryptosporidium
infection in camels (Camelus dromedarius)
in a slaughterhouse in Iran. Trop Biomed
Gharekhani J, Heidari H, Youssefi M. Prevalence of Cryptosporidium
infection in sheep in Iran. Turkiye Parazitol Derg
Nazifi S, Behzadi MA, Haddadi SH, Jahromi AR, Mehrshad S, Tamadon A. Prevalence of Cryptosporidium
isolated from dromedary camels (Camelus dromedarius)
in Qeshm Island, Southern Iran. Comp Clin Path
Ranjbar R, Fattahi R. Prevalence of Cryptosporidium
spp. in calves under one year old in Ilam county (Iran), from March 2014 to February 2015. Electron Physician
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
Shafieyan H, Alborzi A, Hamidinejat H, Tabandeh MR, Hajikolaei MRH. Prevalence of Cryptosporidium
spp. in ruminants of Lorestan province, Iran. J Parasit Dis
Bahrami S, Alborzi AR, Molayan PH, Purbaram S, Mousavi B. Prevalence of Cryptosporidium
spp. infection and its association with diarrhea in buffalo calves in Khuzestan, a southwestern province of Iran. Buffalo Bull
Safavi EA, Mohammadi GR, Naghibi A, Rad M. Prevalence of Cryptosporidium
spp. infection in some dairy herds of Mashhad (Iran) and its association with diarrhea in newborn calves. Comp Clin Path
Radfar MH, Molaei MM, Baghbannejad A. Prevalence of Cryptosporidium
spp. oocysts in dairy calves in Kerman, southeastern Iran. Iran J Vet Res
Yakhchali M, Moradi T. Prevalence of Cryptosporidium
-like infection in one-humped camels (Camelus dromedarius)
of northwestern Iran. Parasite
Yagoob G, Ataollah T, Muhammad F. Prevalence of dog intestinal parasites and zoonotic importance of them in Sarab city, Iran. Cibtech J Zool
Tavassoli M, Dalir-Naghadeh B, Valipour S, Maghsoudlo M. Prevalence of gastrointestinal parasites in water buffalo (Bubalus bubalis)
calves raised with cattle in smallholder farming system in the Northwest of Iran. Acta Vet Eurasia
Norolahi Fard F, Asl N, Rezaei Seghinsara H. Prevalence of intestinal cryptosporidiosis in pigeons in Mashhad. Iran J Vet Clin Sci
Mirzaei M, Mohammadi V, Fotouhi Ardakani R. Prevalence of intestinal Cryptosporidium
infection in Kerman pigeons (short paper). Sci Iran Vet J
Mirzaei M. Prevalence of stray dogs with intestinal protozoan parasites. Am J Anim Vet Sci
Beigi S, Nourollahi Fard SR, Akhtardanesh B. Prevalence of zoonotic and other intestinal protozoan parasites in stray cats (Felis domesticus)
of Kerman, South-East of Iran. Istanbul Univ Vet Fak Derg
Beiromvand M, Akhlaghi L, Fattahi Massom SH, Meamar AR, Motevalian A, Oormazdi H, et al. Prevalence of zoonotic intestinal parasites in domestic and stray dogs in a rural area of Iran. Prev Vet Med
Nouroozi RV. Prevalence of Cryptosporidium
in wild brown rat (Rattus norvegicus)
population at Shoushtar, Iran. Int Electron J Med
Jafari R, Maghsood AH, Fallah M. Prevalence of Cryptosporidium
infection among livestock and humans in contact with livestock in Hamadan District, Iran, 2012. J Res Health Sci
Esmail F, Ataallah H. Prevalence of Cryptosporidium
oocysts from calves in Kurdistan province, of Iran. Internet J Parasit Dis
(2). doi: 10.5580/17a2.
Yagoob G, Bahman K. Prevalence of intestinal protozoan parasites in stray dogs of Tabriz city, Iran. Indian J Fundam Appl Life Sci
Ranjbar Bahadori S, Aliari M. Risk factors for cryptosporidial diarrhea in calves. J Vet Res
Shirazi SH, Hashemzadeh Farhang H, Mirsamadi N, Shahbazi P. Studying the prevalence of cryptosporidiosis among human, calf and wild rat papulations in Tabriz. J Large Anim Clin Sci Res (J Vet Med)
Heidari H, Gharakhani J. Study of Cryptosporidium
infection in the livestock (cattle, sheep, dogs, fowls) and humans, in Hamadan city and its suburbs during 2006-2011. Avicenna J Clin Med
Shemshadi B, Bahadori SR, Mozafari A. Study on cryptosporidiosis incidence in broilers in Garmsar region, Iran. Comp Clin Path
Gharekhani J. Study on gastrointestinal zoonotic parasites in pet dogs in Western Iran. Turkiye Parazitol Derg
Ranjbar-Bahadori Sh, Azizzadeh M, Taghvaei M. Study on the infection rate to Cryptosporidium
in suckling calves of Ghuchan district. Iran Vet J
Changizi E, Salimi-Bejestani MR, Javheri Vayeghan A. The Cryptosporidium ryanae
infection commence in Iranian cattle. J Vet Res
Azami M, Moghaddam DD, Salehi R, Salehi M. The identification of Cryptosporidium
species (protozoa) in Ifsahan, Iran by PCR-RFLP analysis of the 18S
rRNA gene. Mol Biol (Mosk)
Khezri M, Khezri O. The prevalence of Cryptosporidium
spp. in lambs and goat kids in Kurdistan, Iran. Vet World
Afkhamnia MR, Nouri M, Karimi GR, Banani M, Ghadiri Abyaneh M. The report of cryptosporidiosis (Cryptisporidium
infection) in commercial chicken farms of Tabriz area. Vet J
Baghban F, Moradimofrad MA. The survey of abundance of Cryptosporidium
spp. oocysts in diarrhoeic calves in Yasuj city. J Large Anim Clin Sci Res (J Vet Med)
Hashemzadefarhang H, Shahbazi P, Bahavarnia SR. The survey on Cryptosporidium
parasite infection in Tabriz and suburb native poultry. Sci J Manag Syst
Gholipoury M, Rezai HR, Namroodi S, Khazaeli FA. Zoonotic and non-zoonotic parasites of wild rodents in Turkman Sahra, northeastern Iran. Iran J Parasitol
Khurana S, Chaudhary P. Laboratory diagnosis of cryptosporidiosis. Trop Parasitol
Adeyemo FE, Singh G, Reddy P, Stenström TA. Methods for the detection of Cryptosporidium
From microscopy to nucleic acid based tools in clinical and environmental regimes. Acta Trop
Shaposhnik EG, Abozaid S, Grossman T, Marva E, On A, Azrad M, et al. The prevalence of Cryptosporidium
among children hospitalized because of gastrointestinal symptoms and the efficiency of diagnostic methods for Cryptosporidium. Am J Trop Med Hyg
Robinson G, Chalmers RM. Cryptosporidium
diagnostic assays: Microscopy. Methods Mol Biol
1-10. doi: 10.1007/978-1- 4939-9748-0_1.
Taghipour A, Olfatifar M, Foroutan M, Bahadory S, Malih N, Norouzi M. Global prevalence of Cryptosporidium
infection in rodents: A systematic review and meta-analysis. Prev Vet Med
105119. doi: 10.1016/j.prevetmed.2020.105119.
García-Livia K, Martín-Alonso A, Foronda P. Diversity of Cryptosporidium
spp. in wild rodents from the Canary Islands, Spain. Parasit Vectors
Rabiee MH, Mahmoudi A, Siahsarvie R, Kryštufek B, Mostafavi E. Rodent-borne diseases and their public health importance in Iran. PLoS Negl Trop Dis
Cai Y, Zhang NZ, Gong QL, Zhao Q, Zhang XX. Prevalence of Cryptosporidium
in dairy cattle in China during 2008-2018: A systematic review and meta-analysis. Microb Pathog
Odeniran PO, Ademola IO. Epidemiology of Cryptosporidium
infection in different hosts in Nigeria: A meta-analysis. Parasitol Int
Galván-Díaz AL. Cryptosporidiosis in Colombia: A systematic review. Curr Trop Med Rep
Rashid M, Rashid MI, Akbar H, Ahmad L, Hassan MA, Ashraf K, et al. A systematic review on modelling approaches for economic losses studies caused by parasites and their associated diseases in cattle. Parasitology
Razakandrainibe R, Diawara EHI, Costa D, Le Goff L, Lemeteil D, Ballet JJ, et al. Common occurrence of Cryptosporidium hominis
in asymptomatic and symptomatic calves in France. PLoS Negl Trop Dis
Taghipour A, Olfatifar M, Bahadory S, Godfrey SS, Abdoli A, Khatami A, et al. The global prevalence of Cryptosporidium
infection in dogs: A systematic review and meta-analysis. Vet Parasitol
109093. doi: 10.1016/j.vetpar.2020.109093.
Berahmat R, Spotin A, Ahmadpour E, Mahami-Oskouei M, Rezamand A, Aminisani N, et al. Human cryptosporidiosis in Iran: A systematic review and meta-analysis. Parasitol Res
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3]