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. 2018 Mar 19;11(3):332–341. doi: 10.14202/vetworld.2018.332-341

Status of theileriosis among herbivores in Iran: A systematic review and meta-analysis

Masoud Soosaraei 1, Mousa Motavalli Haghi 2, Fariborz Etemadifar 2, Mahdi Fakhar 3,, Saeed Hosseini Teshnizi 4, Hajar Ziaei Hezarjaribi 3, Shabnam Asfaram 1
PMCID: PMC5891849  PMID: 29657426

Abstract

Aim:

Theileriosis is a protozoal disease caused by Theileria spp. mostly in warm-blooded vertebrates worldwide. It is one of the common tick-borne diseases among domestic animals in tropical and sub-tropical regions, which have a variety of unlikable effects on health economy and animal welfare. In the present study, the prevalence of theileriosis among domestic farm animals in Iran was systematically evaluated.

Methods:

To identify the related papers, 10 English and Persian databases, including PubMed, Science Direct, Scopus, Web of Science, Medical Subject Headings, Google Scholar, Magiran, Barakatns (formerly Iranmedex), Elm net, and Scientific Information Database, were appraised for articles published throughout 1999-2017.

Results:

A total of 56 papers, providing the examination of 11,317 cattle, 9394 sheep, 2991 buffaloes, 1504 horses, 600 goats, and 212 donkeys were analyzed, matching for the prevalence of theileriosis from different parts of Iran were permitted for our allowing checklist. The overall prevalence of theileriosis among domestic herbivores was expected to be 19% (95% confidence interval: 15%, 22%). Our findings highlighted the average of the maximum prevalence in Razavi Khorasan (60.4%) and West Azerbaijan (49.1%) and the minimum in Mazandaran (1.1%) and East Azerbaijan provinces (2.2%), respectively. The high prevalence of Theileria infection in the herbivores (mainly sheep) verifies the well-known enzootic episode of theileriosis in Iran, predominantly in northeastern and western parts of the country.

Conclusion:

Our results suggested updated and imperative information on the true burden of theileriosis in Iran. Moreover, it could be supporting the gaps among monitoring, prevention, and control arrangements to improve the health economy, particularly among dairy farm animals.

Keywords: epidemiology, Iran, livestock, systematic review, Theileria spp

Introduction

Theileriosis is a tick-borne hemoprotozoal tropical disease in various warm-blooded vertebrates mainly domestic and wild mammals caused by protozoan parasites belonging to the Theileria spp. [1,2]. Theileria is a genus of protozoan that belongs to the phylum Apicomplexa (order: Piroplasmida and family: Theileriidae), which is transmitted by ixodid hard ticks acting as natural vectors. The parasite life cycle is well-known by extra-erythrocytic merogony in the lymphocytes and histiocytes, following by invasion of the red blood cells by the merozoites [3]. Although, Theileria parasite infect mainly a variety of both domestic and wild livestock, there is no proof that Theileria spp. are threats to human population [2,4,5].

Cattle and buffaloes can be infected by various species of Theileria and infections differ from subclinical (known as mild) to malignant (known as severe). Almost nine mild and malignant species of Theileria causing bovine theileriosis are including Theileria mutans, Theileria buffeli, Theileria orientalis, Theileria velifera, Theileria taurotragi and Theileria parva (as malignant bovine theileriosis; known as East Coast fever), Theileria annulata (known as tropical bovine theileriosis), Theileria sergenti, and T. taurotragi, respectively. Likewise, at least seven spices including Theileria lestoquardi (formerly Theileria hirci), Theileria luwenshuni, Theileria uilenbergi (causing malignant ovine theileriosis), and Theileria separata, Theileria ovis, Theileria recondita (causing mild ovine theileriosis), and T. annulata are naturally causal agents of ovine theileriosis with worldwide distribution [6]; although recently, T. annulata, as causal agent of malignant bovine theileriosis, has been reported in southern Iran [7,8].

Laboratory diagnosis of theileriosis was performed mostly by detecting schizonts in Giemsa-stained thick and thin smears from blood or lymph node fine needle aspiration. Several conventional and novel diagnostic tools vary from low to high sensitivity, such as polymerase chain reaction (PCR) test, enzyme-linked immunosorbent assays (ELISAs), or an indirect fluorescent antibody test (IFAT), were used for determining prevalence and differentiating the Theileria spp. [6,9-11]. In spite of the presence of a variety of studies concerning theileriosis among livestock in Iran, there is inapplicable data about the true burden of it in these animals to forecast the financial burden and well-known capacity for control and prevention planning.

Concerning the influences of theileriosis on economy and animal welfare, more deliberations would be crucial for the epidemiological aspects and the approaches to screening panels in Iran. To the best of our knowledge, there is no systematic review and meta-analysis on the subject of animal theileriosis in Iran; thus, the main goal of our study was to find out the present status of ovine, bovine, and equine theileriosis in the country.

Methods

Ethical approval

Ethical approval is not needed for this kind of study.

Searching approach

For searching purpose, 10 English and Persian databases, including PubMed, Science Direct, Scopus, Web of Science, Medical Subject Headings, Google Scholar, Magiran, Barakatkns (formerly Iranmedex), Elm net, and Scientific Information Database, were chosen during 1999-2017. To exploring the articles, the terms including: Theileria, Theileriosis, T. orientalis, T. annulata, T. hirci, T. lestoquardi, T. ovis, Theileria equi, cattle, buffalo, bovine, sheep, goat, ovine, caprine, horse, donkey, equine, and “Iran” alone or in combination were used. To avoid the risk of selection bias in this study, the inclusion criteria were clearly classified and studied. Experimental studies, clinical trials, duplicates, case reports, monkey, carnivores, camel, and studies out of Iran were expelled. All descriptive studies corresponding to the prevalence of ovine, bovine, and equine theileriosis were reviewed. The stages of the study plan are briefly explained in Figure-1.

Figure-1.

Figure-1

Flow diagram of classification of papers for inclusion in this systematic review and meta-analysis.

Data extraction

The data were extracted from the included studies by four reviewers (M. Soosaraei, M. Motavalli Haghi, F. Etemadifar, and Sh.Asfaram), who used a standard form. Any disagreement was resolved by discussion between the four reviewers. If consensus could not be reached, two reviewers were consulted (M. Fakhar and H. Ziaei Hezarjaribi). The kappa index showed an agreement of 89% between the fives reviewers. The standard form consisted of the following variables: First author; year of publication, year of study, type of animal, place of conducted survey (Province), sample size, number of positive, and diagnostic laboratory methods (Table-1) [7,12-65]. The quality of selected studies was assessed using the STROBE scale (score under 7.75 low quality, 7.76-15.5 moderate and 15.6-23.5 moderate to height, and upper 23.6 height quality).

Table-1.

Baseline features of included studies.

Animal No. of examined No. of positive Species Laboratory method Place (province) References
Sheep 1000 92 T. lestoquardi Microscopy Fars [12]
Buffalo 2700 82 T. annulata Microscopy Khouzestan [13]
Cattle 372 216 T. annulata Microscopy Razavi Khorasan [14]
Sheep 300 29 T. lestoquardi Microscopy Lorestan [15]
Cattle 390 15 Theileria Microscopy Chaharmahal va Bakhtiari [16]
Sheep 300 39 Theileria Microscopy Mazandaran [17]
Cattle 124 61 Theileria ELISA West Azerbaijan [18]
Sheep 200 7 Theileria spp. Microscopy Mazandaran [19]
Sheep 840 100 Theileria spp. Microscopy South Khorasan [20]
Cattle 600 34 T. annulata Microscopy Sistan and Baluchestan [21]
Cattle 252 26 T. annulata Microscopy Sanandaj [22]
Cattle NR NR T. annulata Semi-nested PCR Tehran, Fars, Sistan, and Baluchestan [23]
Sheep 150 71 Theileria spp., T. ovis, T. lestoquardi PCR Sistan and Baluchestan [24]
Sheep 100 60 Theileria spp., T. lestoquardi PCR South Khorasan [25]
Cattle 160 110 Theileria spp., T. annulata Microscopy Razavi Khorasan [26]
Sheep 100 56 T. ovis, T. lestoquardi PCR East and South-East provinces [27]
Sheep 470 21 T. lestoquardi, T. ovis PCR 10 various regions of Iran [28]
Sheep 220 181 T. lestoquardi, T. ovis PCR and microscopy 5 various regions in eastern half of Iran [24]
Cattle 160 16 T. annulata and T. orientalis Semi-nested PCR Golestan [29]
Sheep 200 11 T. ovis Microscopy West Azerbaijan [30]
Cattle 100 22 T. annulata IFAT West Azerbaijan
Cattle 160 20 T. annulata PCR Golestan [31]
Cattle T. annulata PCR-RFLP Kurdistan and West-Azerbaijan [32]
Cattle 200 63 T. annulata Microscopy Kerman [33]
Sheep 250 101 T. lestoquardi and T. ovis Nested PCR Western half of Iran (Sari, Rasht, Urmia, Ilam, and Ahvaz) [7]
Cattle 52 19 T. annulata PCR-RFLP Azerbaijan [34]
Cattle 52 30 T. annulata PCR-RFLP Kurdistan and Kermanshah
Cattle 1202 706 T. annulata PCR Isfahan, Khuzestan, Chaharmahal va Bakhtiari, Kohgiluyeh va Boyer Ahmad and Lorestan [35]
Cattle 160 34 T. orientalis and T. annulata Semi-nested PCR Golestan [36]
Sheep 165 9 T. annulata and T. ovis PCR Tehran [37]
Sheep 568 73 Theileria spp. Microscopy Ilam [38]
Sheep 100 12 Theileria spp. Microscopy Lorestan [39]
Sheep 300 6 Theileria spp. Microscopy Tehran [40]
Sheep 100 46 T. ovis and T. annulata Semi-nested PCR Fasrs [41]
Sheep 90 68 T. ovis and T. lestoquardi Semi-nested PCR North Khorasan [42]
Sheep 452 295 T. ovis, T. lestoquardi and T. annulata Semi-nested PCR Razavi Khorasan [43]
Cattle 176 42 Theileria spp. PCR Isfahan [44]
Cattle 270 20 T. annulata PCR Yazd, North Khorasan and Mazandaran [45]
Horses 165 47 T. equi PCR Khuzestan [46]
Horses 240 41 T. equi PCR West Azerbaijan [47]{Malekifard, 2014 #2067}{Malekifard, 2014 #2067;Malekifard, 2014 #2067}
Horses 100 53 T. equi IFAT North Khorasan [48]
Horses 205 45 T. equi PCR North Khorasan and Yazd [49]
Sheep 119 106 Theileria spp. PCR Khuzestan [50]
Cattle 150 43 Theileria spp. PCR Isfahan [51]
Donkeys 106 54 T. equi Multiplex-PCR North Khorasan [52]
Cattle 138 13 T. annulata PCR Kermanshah [53]
Horses 59 21 T. equi PCR Khuzestan [54]
Sheep 150 19 T. lestoquardi and T. ovis PCR Lorestan [55]
Cattle 150 84 T. annulata PCR Kerman [56]
Cattle 100 4 T. annulata PCR Yazd [57]
Goats 100 0 Theileria Microscopy Razavi Khorasan [58]
Sheep 80 59 Theileria PCR Sistan and Baluchestan [59]
Cattle 160 60 T. annulata PCR Sistan and Baluchestan [60]
Cattle 138 37 Theileria Semi-nested PCR West Azerbaijan [61]
Goat 400 39 T. lestoquardi PCR West Azerbaijan [62]
Cattle 193 76 T. annulata and T. orientalis Molecular assays West Azerbaijan [63]
Buffalo 291 10
Cattle 51 2 T. lestoquardi and T. annulata PCR Khuzestan [64]
Horse 90 10 T. equi PCR Isfahan and Shahrekord [65]

NR: Not reported, T. lestoquardi=Theileria lestoquardi, T. annulata=Theileria annulata, T. ovis=Theileria ovis, T. orientalis=Theileria orientalis, T. equi=Theileria equi, PCR=Polymerase chain reaction, IFAT=Indirect fluorescent antibody test, ELISA=Enzyme-linked immunosorbent assays, RFLP=Restriction fragment length polymorphism

Effect measures

The outcome was the prevalence of Theileria, and this was obtained for each study by dividing the number of positive cases by the total sample size.

Statistical analysis

The prevalence of each study was collected, and according to the binomial distribution, standard error Inline graphic for each study was calculated and the inverse of SE each study considered as the weight of that study. The effect size (ES) for each study and pooled outcome revealed as a forest plot (reported as ES with a 95% confidence interval [95% CI]). Cochran’s heterogeneity statistics based on Chi-square test Q-test (p<0.1 as heterogeneities) and the I2 statistic which describes the percentage of variation across studies (values of 25%, 50%, and 75% indicate low, moderate, and high degrees of heterogeneity, respectively). At present heterogeneity, random effects model (Der Simonian Laird model) and otherwise applied fixed-effect model (Mantel Haenszel) were used to compute overall ES. Subgroup analyses were performed to investigate potential sources of heterogeneity from different sex and age. Egger’s tests were used to evaluate publication bias. All statistical analyses were fulfilled with the statistical software package (Stata) version 11.1. (Stata Corp LP, College Station, TX, USA). p<0.05 was measured statistically significant.

Results

Among each one of the databases investigated during 19 years from 1999 to 2017, overall 56 articles were fitting to be integrated into our systematic review and meta-analysis. All papers were assigned and assessed the prevalence of theileriosis among herbivores including sheep, goat, cattle, buffalo, horse, and donkey in Iran. Absolutely, 11,317 cattle, 9394 sheep, 2991 buffaloes, 1504 horses, 600 goats, and 212 donkeys were analyzed, respectively. In general, because of the restricted data fulfilled on camel theileriosis in Iran, we included just articles correlated to the disease among domesticated herbivores except for camel.

The mean of scores for the STROBE scale was to be found 21.73 which performed quality of these studies was moderate to height. As indicated by a random effect meta-analysis (I2=98.94%, p<0.001) the pooled event of Theileria infection in Iran was acquired 19% (95% CI: 15%, 22%). The prevalence rate of ovine (sheep and goats), bovine (cattle and buffaloes), and equine (horses and donkeys); theileriosis was 23.0% (17.0-30.0%), 14.0% (11.0-19.0%), and 20.0% (11.0-30.0%), respectively; a significant statistically difference was observed among them (z=5.80, df=2, p=0.05) (Figures-2 and 3).

Figure-2.

Figure-2

Detailed presentation of overall distribution of Theileria spp. infection in the provinces of Iran.

Figure-3.

Figure-3

Estimate of the prevalence of Theileria infection among herbivores based on 56 studies in different years and areas in Iran. The pooled random effect size and 95% confidence interval represents by diamond, 19% (15-22%). Overall heterogeneity based on random effect model was showed by I2 (97.94%, p<0.001). The vertical dash line represents overall estimate, and the vertical solid line represents the value of null hypothesis.

Besides, our results showed the prevalence of Theileria infection among sheep (23%) which was considerably too much than other herbivores (p<0.001); and prevalence of T. ovis and T. annulata in sheep and cattle was significantly higher than other ones, respectively (p<0.001).

In addition, the highest prevalence of T. equi infection in horses 19.0% (11.0-29.0%) was detected by IFAT (51%) and the lowest by microscopic methods (7%). There was significant difference between prevalence of laboratory methods which used for diagnosing equine theileriosis for horses (Q-test=137.25, df=2, p<0.001).

The subgroup analysis showed PCR method had the most prevalence for sheep, 33.0% (95% CI: 20.0-48.0%) and a significant difference between prevalence of Theileria infection and laboratory techniques used among sheep (Q-test=9.5, df=3, p=0.02). Moreover, our meta-analysis showed a significant difference among Theileria species in sheep (Q-test=41.2, df=3, p<0.001) and cattle (Q-test=180.43, df=4, p<0.001), correspondingly. In addition, the analysis confirmed a significant difference between prevalence of Theileria infection and laboratory methods used for cattle (Q-test=699.32, df=5, p<0.001).

The results of Egger’s test for each of animal subgroups provided no evidence of publication bias in the studies (p>0.1) (Table-2). Therefore, it appears that both studies with low and high prevalence were contributed in this meta-analysis. The consequences of subgroup examination independently for type of laboratory methods and Theileria spp. infection showed that these two elements are two major sources of heterogeneity among prevalence of theileriosis for studies related to cattle and sheep, except horses.

Table-2.

The results of Egger’s test to assess publication bias.

Animals Number of studies bias p
Cattle 25 1.08 0.21
Sheep 24 1.37 0.56
Horses 7 2.30 0.11
Overall 56 1.67 0.13

Discussion

Our study is the first systematic review on theileriosis in Iran. Theileriosis is an economically important protozoal disease among domesticate livestock in Iran with overall 19% infection rate, and the infection rates in sheep are 23%, which cause terrible impacts on the economy. The disease is widespread and well known in several parts of Iran, which affects animals’ husbandry and their productions in the country. The majority cases of theileriosis occurred in June-July and the lowest in March-April in northwestern and southeastern Iran [4,66]. In addition, the high prevalence of ovine theileriosis in different areas of Iran is probably identified with a few issues, for example, vector seasonal frequency, weather and environmental alterations, host susceptibility, ticks resistance to insecticide, high frequency of tick-infested in sheep versus cattle, and insufficient preventive policies. [4,67-70].

Several hard tick genera including Amblyomma, Haemaphysalis, Hyalomma, and Rhipicephalus as main vectors of theileriosis are scattered in all ruminant grazing lands, and accordingly, the chance of transmission of it is increased [48].

In our study, the pooled prevalence of livestock theileriosis is approximated to be 19% in Iran. Moreover, the prevalence rate of theileriosis in various geographical regions demonstrated that there were assorted zones in Iran with high prevalence rates in cattle with 58% in Razavi Khorasan, northeastern, and 57.6% in Kermanshah, western Iran, in sheep with 71% in Sistan and Baluchestan, Eastern, 70%, 55.6% in North Khorasan and Razavi Khorasan, respectively; in horses with 53% in North Khorasan provinces. Furthermore, the average prevalence of infection rate was notably lower in the central and northern provinces of the country.

Our findings are in symmetry with a study carried out on sheep and goats in Pakistan, eastern neighborhood of Iran, in 2012, by microscopic examination, 11.2% samples were positive for Theileria spp. The prevalence of Theileria spp. was 13.9 % and 8.2% in sheep and goat, respectively [71].

In Turkey, as western neighborhood of Iran, the prevalence of T. buffeli/T. orientalis was reported between 0.9% and 13.6% using PCR, and T. annulata was reported between 0% and 60.5% using microscopic method. The seroprevalence of T. annulata was found between 1.8% and 91.4% by IFAT. The prevalence of T. annulata by molecular techniques was between 15.4% and 61.2%. The prevalence of T. recondita/T. ovis by microscopic examination of thin blood smears was varied from 0% to 41.3% and its seroprevalence was found to be between 8.2% and 63.2% by IFAT. Weather conditions, the tick seasonal activities, and ecological conditions of Turkey and Kurdistan region of Iraq are extremely close to western and northwestern Iranian provinces, e.g., West and East Azerbaijan [32,72-75].

On the whole, our study showed that the average prevalence rate of ovine, bovine, and equine theileriosis was 23, 14, and 20%, respectively. In this study, five species of Theileria were identified which abundantly found in different livestock, would be considered as causal agents of theileriosis in the country. Our data showed that ovine theileriosis caused by T. lestoquardi infection is common in southern, southwestern, and southeastern parts of Iran and T. ovis is prevalent all over the country; even though the latest species is the main species in northern, western, and northwestern areas of Iran [7,24,43].

Regarding bovine theileriosis in Iran, our data are similar to the prior epidemiological surveys of T. orientalis and T. annulata in neighboring countries. For example, in four districts of Punjab, Pakistan, the pooled prevalence of T. orientalis was approximately 24.5, 6, and 6.1% by multiplexed tandem PCR method in the imported and native Pakistani cattle and buffaloes, respectively [76].

Equine theileriosis is caused due to T. equi and Babesia caballi and it is widespread in the most of tropical parts of countries in Europe, Africa, Asia, and countries surrounding Iran such as Turkey [77,78], Oman [79], Saudi Arabia [80], Kuwait [81], United Arab Emirates [82], and Iraq [83] as well as from other countries, found varying degrees of parasite prevalence. Overall, T. equi is most common and malignant than T. caballi in many endemic parts of the world including Iran [49].

In a study from Iran, with PCR assay showed infection with T. equi in 50.9% of the donkeys [52]. The frequency of T. equi infections was recorded from 31.8% of donkeys in Brazil using PCR method [84], 0.5-12% of blood smears of donkeys in Ethiopia [85-89]. Seropositivity rates of T. equi infection were in73.8% of donkeys in Brazil [84], 55.7% in Ethiopia [87], 9.6% in China [88], 47.2% in Spain [89], and 4-13% in Turkey [90,91].

Our findings and recent data show that T. equi and T. caballi were common in horse populations in provinces of Iran including East and West Azerbaijan, North Khorasan, and Khuzestan [23,47].

Herbivores theileriosis is answerable for high mortality and morbidity of livestock and subsequently fizzling economy, stunning effects on traditional and industrial animal breeding, in addition falling control approaches [4,92].

The diagnosis of theileriosis is based on traditional methods including microscopic examination (mostly thick and thin Giemsa-stained blood smears), and clinical symptoms. On the other hand, since the microscopic method has low sensitivity, this technique is not being reliable for the detection of asymptomatic and or subclinical infections because of the low parasitemia and or low virulence [6,93]. Moreover, serological assays such as ELISA and IFAT have also many disadvantages such as cross-reactivity between various species. Recently, molecular tools have picked up notoriety and prominence for detection and characterization proof of various pathogens. Altogether, serological and molecular tools may be appropriate in mild and also asymptomatic and or subclinical infections [6,93-95].

Given that there is a large number of studies about distribution status of ruminant theileriosis contrasting babesiosis [62] and a limited number of studies regarding equine theileriosis in Iran. Moreover, the most of studies are concentrated on ovine theileriosis, so an urgent need for updated data about the prevalence of theileriosis in Iranian equine theileriosis would be required. Nonetheless, a few unpublished data concerning ovine and bovine theileriosis are available in local provincial veterinary health and management centers gathered from private veterinary clinics and diagnostic laboratories in the various parts of Iran, which even though they are not exactly noteworthy and valid for appraisal.

Conclusion

The high occurrence of Theileria infection in domestic livestock in Iran, frequently among sheep, confirm the endemic and stable situations of theileriosis in the studied regions particularly northeastern and western provinces of the country and maybe a warning for animal welfare and health economy. In brief, our data offer valuable and encouraging information as regards the current situation of theileriosis in domestic herbivores in Iran, which might be useful for active and passive surveillance and preventing plans for the disease. Further investigation and monitoring will be needed to expand the surveillance and control policies, such as quite vaccination full coverage and improvement the traditional diagnostic tools and assessment the pesticide resistance in ticks to reduce the mortality and morbidity of theileriosis among livestock and consequently decrease the risk of outbreaks and economic failure and public health hazardous in Iran.

Authors’ Contributions

MS, MMH, FE, and SA made searching strategy paper selection and wrote the manuscript draft, MF and HZH designed all steps of the study, SHT analyzed the extracted data. All authors read, revised, and approved the final manuscript.

Acknowledgments

The Vice Chancellor of Research and Technology, Mazandaran University of Medical Sciences, Iran provided funding for this systematic review and meta-analysis (grant number: 2980).

Competing Interests

The authors declare that they have no competing interests.

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