A comprehensive systematic review and meta-analysis study

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Epidemiology of brucellosis in Iran: A comprehensive systematic review and meta-analysis study

Article in Microbial Pathogenesis · June 2017

DOI: 10.1016/j.micpath.2017.06.005

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Epidemiology of brucellosis in Iran: A comprehensive systematic review and meta-analysis study

Reza Mirnejad

^a

, Faramarz Masjedian Jazi

^b

, Shayan Mostafaei

^c^,^d

, Mansour Sedighi

^b^,^*

aMolecular Biology Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran

bDepartment of Microbiology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran

cRheumatology Research Center, Tehran University of Medical Sciences, Iran

dDepartment of Biostatistics, School of Medical Sciences, Tarbiat-Modares University, Tehran, Iran

a r t i c l e i n f o

Article history:

Received 24 May 2017 Received in revised form 3 June 2017

Accepted 6 June 2017 Available online 7 June 2017

Keywords:

Brucellosis Epidemiology Systematic review Meta-analysis Iran

a b s t r a c t

Brucellosis is still one of the most challenging issues for health and the economy in many developing countries such as Iran. Considering the high prevalence of brucellosis, the aim of the current study was to systematically review published data about the annual incidence rate of this infection from different parts of Iran and provide an overall relative frequency (RF) for Iran using meta-analysis. We searched several databases including PubMed, ISI Web of Science, Scopus, google scholar, IranMedex and Iranian Scientiﬁc Information Database (SID) by using the following keywords:“Brucella”,“Brucellosis”,“Malta fever”,“Mediterranean fever”,“undulant fever”,“zoonosis”and“Iran”in Title/Abstract/Keywordsﬁelds.

Articles/Abstracts, which used clinical specimens and reported the incidence of brucellosis, were included in this review. Quality of studies was assessed by STROB and PRISMA forms. All statistical analyses were performed using STATA 11.0 (STATA Corp, College Station, TX) andP-values under 0.05 were considered statistically signiﬁcant. Out of the 8326 results, we found 34 articles suitable, according to inclusion and exlusion criteria, for inclusion in this systematic review and meta-analysis. The pooled incidence of brucellosis was estimated 0.001% (95% conﬁdence interval (CI)¼0.0005e0.0015%) annually.

Relative frequency of brucellosis in different studies varied from 7.0/100000 to 276.41/100000 in Qom and Kermanshah provinces, respectively. This systematic-review and meta-analysis study showed that the highest incidences of brucellosis are occurred in west and northwest regions of Iran. Totally, the incidence of the disease in Iran is in the high range.

Contents

1. Introduction . . . 240

2. Materials and methods . . . 240

2.1. Search strategy . . . 240

2.2. Study selection . . . 241

2.3. Quality assessment . . . 241

2.4. Data extraction . . . 241

2.5. Inclusion criteria . . . 242

2.6. Exclusion criteria . . . 242

2.7. Statistical analysis . . . 242

3. Results . . . 242

4. Discussion . . . 243

*Corresponding author. Department of Microbiology, School of Medicine, Iran University of Medical Sciences, Tehran 1439914153, Iran.

E-mail addresses:[email protected](R. Mirnejad),[email protected] (F.M. Jazi), [email protected] (S. Mostafaei), mansour.sedighi60@

yahoo.com(M. Sedighi).

Contents lists available atScienceDirect

Microbial Pathogenesis

j o u r n a l h o m e p a g e :w w w . e l s e v i e r . c o m / l o c a t e / m i c p a t h

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5. Conclusion . . . 245

Ethical approval . . . 245

Funding . . . 245

Authors' contribution . . . 245

Conflict of interest . . . 245

Informed consent . . . 245

Acknowledgement . . . 245

References . . . .. . . 246

1. Introduction

Brucellosis, also known as “undulant fever”, “Mediterranean fever”, “Malta fever”, “Gibraltar fever”, “thousandface disease”,

“raging fever”or“melitococci disease”, is an important world-wide disease in both human and animals that caused by Gram-negative bacteria,Brucellaspp.[1,2]. Human might be infected byBrucella abortus,Brucella canis,Brucella suisandBrucella melitensis. Infection intensityBrucellatypes such thatB. abortusandB. caniscause to mild disease while in brucellosis caused byB. suis, the duration is longer and symptoms are more severe.Brucella melitensisis the most abundant and acute type followed by different disturbances [3,4]. Brucellosis is almost transmitted by indirect or direct contact with infected animals or their products, invariably so known as zoonotic disease[5]. The disease affects people of all age groups and of both men and women, worldwide [6]. The disease is a major public health issue throughout the world and one of the most so- cioeconomic problems in many developing countries, especially in the Mediterranean basin, north and east Africa, the Middle East, the Arabian Peninsula, the Indian subcontinent and parts of South America and central Asia[7]. In these areas, poor diagnosis and treatment may result in serious complications[8]. Brucellosis is a contagious, costly disease of ruminant animals that also affects humans[5,7]. According to the WHO reports, annually more than 500,000 incident cases of brucellosis are notiﬁed worldwide especially from developing countries, and that for every case diagnosed with the disease, four cases go undetected[9e12]. Dairy products, climatic situation, environmental hygiene, and socio- economic conditions are main factors of infectiousness and transmission of brucellosis. Human contact with infected animals is the most common mode of transmission[13]. There is a considerable variation in the frequency of brucellosis in different parts of Iran.

The incidence varied between 98 and 130 per 100,000 populations.

Southern parts of Iran have the lowest incidences of this infection [14]. Human brucellosis is a disease with a wide range of clinical signs, presenting various diagnostic difﬁculties because its symptoms are similar to those of many other diseases[15]. The impor- tance of this disease is not limited to physical complications, and it is considered to be one of the most important challenges for economic development in many countries such as Iran, whose economic growth and employment still depend on livestock and agriculture[16e18]. Iran stands in the second rank regarding the prevalence of Malta fever worldwide[19]. Most common symptoms of brucellosis include undulant fever, weakness, night sweats with peculiar odor and chills[20]. The wide spectrum of brucellosis symptoms in human has led to the fact that diagnosed people are considerably less than the actual number of the infected population [21,22]. Each year, more than 500,000 new cases are reported, and thisﬁgure underestimates the magnitude of the problem[23]. This disease causes high clinical morbidity and various clinical manifestations in humans such as fever, arthralgia and sweating, and any organ can be affected include encephalitis, meningitis, spondylitis,

orchitis, prostatitis, arthritis and endocarditic [24]. Although brucellosis in domestic animals has been controlled in most developed countries, it remains an important public and animal health problem in the developing countries. The disease is endemic in Iran[25].

Due to serious and destroying complication of this infection, early and fast diagnosis and proper treatment of this infection can prevent from the following disabilities[26]. Quality of veterinary service, availability of economic resources, spread of the disease, type of husbandry and the degree of involvement of ranchers are most important factors that should be considered in adopting brucellosis control/eradication programs. Iran is an endemic area for brucellosis which is a serious public health issue in the country [27,28]. This infection is a very important health problem in Iran and according to the data derived from active surveillance during 2001e2005, the incidence of the disease are 120e400 per 100,000 people[29]. According to the annual report of Center for Disease Control in Iran, the incidence rate of brucellosis was 39 per 100,000 and 30 per 100,000 populations in 2005 and 2007, respectively. In addition, the incidence rate of infection has increased to 130 per 100,000 populations in west of Iran in last years. The incidence rate of this infection was 45 per 100,000 populations in Hamadan in 2008[30e32]. One of the important reasons of increasing rate of brucellosis is disability in control of disease in animals. In addition, different clinical manifestations of brucellosis in humans and dif- ﬁculty in deﬁnite diagnosis of the disease caused the incidence rate to be under estimated[21,22].

A database review indicates that numerous studies are carried out on the epidemiological features of Malta fever in Iran. An authentic measurement for the epidemiological and clinical features of Malta fever can be developed through combination of the researchﬁndings using meta-analysis[33]. Furthermore, through systematic review and meta-analysis of the results, we can provide well-groundedﬁndings that can be used in public health policy- making and proposing suggestions for further research[34]. The current research aimed to study the epidemiological features of brucellosis in Iran through carrying out a meta-analysis.

2. Materials and methods 2.1. Search strategy

International databases (ISI Web of Science, PubMed, Scopus, google scholar and Science Direct) and four national scientiﬁc search engines including Medlib (www.medlib.ir), Magiran (www.

Magiran.com), Iranian Scientiﬁc Information Database (www.sid.ir) and “IranMedex” (www.iranmedex.ir) for relevant articles were searched (up to July 2016) by using the following keywords:

“Brucellosis”, “Brucella”, “incidence”, “epidemiology”, “undulant fever”, “Mediterranean fever”, “Malta fever”, “Gibraltar fever”,

“thousand face disease”,“raging fever”,“melitococcis disease”and

“Iran” and their Farsi equivalents within titles and abstracts in R. Mirnejad et al. / Microbial Pathogenesis 109 (2017) 239e247

240

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combination with“OR”and“AND”Boolean Operators in the Title/

Abstract/Keywordsﬁelds. No limitation was used while searching databases. References lists of all related studies were also reviewed for any other related publication. One of the team researchers randomly evaluated the search results and reported that no relevant study was ignored. We also reviewed non-electronic evidence and interviewed with relevant experts and research centers to identify any gray literature. The search was restricted to original Articles/abstracts published in English and Persian that reported the annually incidence rate of brucellosis in different regions of Iran country. Two authors (RM and MS) conducted all these steps and any disagreements with article selection were resolved through discussion, and a third author (FM) was available to resolve the disagreement[35].

2.2. Study selection

We extracted full texts or abstracts, documents and reports of all evidence identiﬁed during our advanced search. After excluding duplicates, we omitted irrelevant studies reviewing titles, abstracts and full texts of papers, respectively. To minimize the reprint bias,

we tried to investigate all results in detail and remove any repeated studies[35].

2.3. Quality assessment

The quality of the relevant articles was evaluated using the STROBE checklist (Strengthening the Reporting of Observational Studies in Epidemiology) [36] and another checklist used in a literature review [37]. Items related to study type, sample size, research objectives, population and inclusion/exclusion criteria for primary research, analysis method, and appropriate presentation of results were determined and a score was assigned to each item. One score was assigned to each question and studies achieved at least eight quality scores were considered eligible for ﬁnal meta- analysis.

2.4. Data extraction

For all studies, the following data were extracted: last name of theﬁrst author, publication date, sample size, study setting, study enrollment time, the relative incidence (RI) of brucellosis and

Fig. 1.Flowchart for literature search and study selection.

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research location. Two authors extracted data from all of the included studies, independently. Inconsistencies between the re- viewers were discussed to obtain consensus.

2.5. Inclusion criteria

Among English and Persian articles/abstracts found with above strategies, those with the following features were included in the study: annually incidence of brucellosis reported from urban and rural different areas of Iran and this infection declared by researchers, hospitals and health centers of Iran, because this review study is limited to Iran country and the purpose of the present study was to measure the incidence of brucellosis in Iran only.

2.6. Exclusion criteria

Articles were excluded from the review if: [1] Studies that did not report the epidemiological features of Malta fever, those with unknown incidence rate and studies published before 1990 were not included. [2] Review articles, case reports, case-control studies and studies that did not score the minimum in quality assessment, were excluded. [3] Finally, congress or conference abstracts that did not include article full text, studies reported in languages other than English or Persian, meta-analyses or systematic reviews and duplicate publication of the same study (or published both in En- glish and Persian) were also excluded.

2.7. Statistical analysis

The numbers of total participants and participants with brucellosis were used to estimate the relative frequency (RF) which

was then converted to log RF and its standard error (SE) for the meta-analysis. The pooled annually incidence rate was derived by random effect model (inverse variance method) that takes between-study variation into account. The heterogeneity and the variation in pooled estimation were assessed by using Cochran's Q test and I-squared, respectively[38]. In order to examine the value which, the pooled incidence might depend on, sensitivity analysis was used for a particular study or a group of publications. Publi- cation bias was checked by Egger's regression asymmetry test and Begg's adjusted rank correlation test[39,40]. All statistical analyses were performed using STATA 11.0 (STATA Corp, College Station, TX) andP-values under 0.05 were considered statistically signiﬁcant.

3. Results

A total of 8326 articles were retrieved by the database search.

Summary of the literature search and study selection showed in Fig. 1. In aﬁrst screening process, 4275 of papers were excluded due to duplication, and 4051 articles were retained for title and abstract assessment. In a secondary screening process, 3674 of publications were excluded based on title and abstract evaluation, and 377 articles were retained for detailed full-text evaluation. After full-text evaluation, 34 articles (abstract with full-text articles) describing the incidences of brucellosis in Iran country were selected for analysis that are presented inTable 1. In studies that we investigate brucellosis infection, infectious specimens take from patients and hospitalized patients in male/female and over ages. As it is clear, most of the studies were conducted in west and northwest of Iran followed by the central.Fig. 2shows the distribution of brucellosis in different parts of Iran. The status of the infection in Iran is rep- resents in Table 2. By using random-effect models, the pooled

Table 1

Characteristics of studies included in the systematic review and meta-analysis after full evaluation.

ID study First author Enrollmenttime publication year Location Incidence rate sample size Ref.

1 Kassiri et al. 2007e2008 2011 Lorestan 56.55/100000 41 [41]

2 Dastjerdi et al. 2006e2011 2012 Isfahan 12.1/100000 1996 [16]

3 Sayyad et al. 2008e2009 2014 Kurdistan 10.9/100000 48 [42]

4 Haghdoost et al. 2001e2004 2007 Kerman 141.6/100,000 97 [43]

5 Hasanzadeh et al. 2003e2010 2013 Isfahan 12.0/100000 139 [44]

6 Ghasemi et al. 1997e2001 2003 Kurdistan 23.48/100000 1591 [45]

7 Esmaeilnasab et al. 2006e2007 2007 Kurdistan 73.5/100000 1059 [46]

8 Mohammadian et al. 1999e2012 2014 Isfahan 52.96/100000 554 [47]

9 Sahargahi et al. 2006e2010 2014 Kermanshah/Eslam Abad-e-Gharb 42e76.4/100000 458 [48]

10 Sahargahi et al. 2006e2010 2014 Kermanshah/Kermanshah 37.4e56.3/100000 458 [48]

11 Hosseini et al. 2004e2005 2009 Southern Khorasan 113.2/100000 115 [49]

12 Mosavi et al. 2008e2010 2014 Kermanshah 42.87/100000 470 [50]

13 Rajabzadeh et al. 2006e2011 2013 Northern Khorasan 26.6/100000 1310 [51]

14 Soleimani et al. 2001e2005 2012 Eastern Azerbaijan 27-113/100000 5732 [52]

15 Soleimani et al. 2005e2009 2012 Eastern Azerbaijan 45.0/100000 5732 [52]

16 Maleki et al. 2008e2012 2015 Western Azerbaijan 102.86/100000 492 [53]

17 Hamzavi et al. 2011 2014 Kermanshah 39.9/100000 777 [54]

18 Shoraka et al. 2008e2009 2010 Northern Khorasan 31.9/100000 64 [14]

19 Kassiri et al. 2008e2009 2013 Lorestan 59.31/100000 43 [55]

20 Almasi et al. 2004e2010 2012 Kermanshah 276.42/100000 210 [56]

21 Farahani et al. 2001e2010 2012 Markazi 60.0/100000 3880 [57]

22 Rostami et al. 2001e2009 2015 different parts of Iran 29.83/100000 1698 [58]

23 Farahbakhsh et al. 2006e2007 2012 Eastern Azerbaijan 113.0/100000 0 [59]

24 Soﬁan et al. 2005 2008 Tehran 17.5/100000 300 [60]

25 Haji-Abdolbaghi et al. 2001 2008 Kurdistan 107.5/100000 0 [61]

26 Rahnema et al. 2001e2005 2005 Golestan 40.0/100000 0 [62]

27 Moniri et al. 1996 1997 Isfahan 90.0/100000 2376 [63]

28 Moradi et al. 2002e2008 2009 Hamadan 65.5/100000 0 [32]

29 Rezaei et al. 2010e2014 2015 Qom 7.0/100000 406 [64]

30 Nowrouzi et al. 2001e2011 2012 Qom 10.8/100000 1253 [65]

31 Iran CDC 2001e2005 2007 Hamedan and Zanjan 98e130/100000 0 [66]

32 Eini et al. 2011 2012 Hamedan 130.0/100000 230 [67]

33 Bokaie et al. 2001e2004 2009 Western Azerbaijan 175.0/100000 640 [68]

34 Bokaie et al. 2002e2006 2008 Southern Khorasan 37.0/100000 176 [69]

R. Mirnejad et al. / Microbial Pathogenesis 109 (2017) 239e247 242

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incidence of brucellosis was estimated 0.001% (95% conﬁdence interval (CI)¼ 0.0005e0.0015%) (Fig. 3). However, evident heterogeneity of Brucellosis RF was not observed among several studies (Chochran Q test,P-value< 0.994 and I squardy0.0%).

Fig. 3shows the forest plot of Meta-analysis of brucellosis. Sensi- tivity analysis was performed by sequential omission of individual studies. The combined RFs of the incidence rate of brucellosis from sequential omission were not altered after omission, indicating that our results were statistically robust (Fig. 4). No publication bias was observed in the Begg's adjusted rank correlation test (P- values¼0.2). However, the Egger's regression test shown signiﬁ- cant publication bias (P-values<0.03) (Fig. 5).

4. Discussion

Brucellosis remains endemic in most areas of the world although in much of Northern Europe, Australia, the US and Canada

it has been eradicated or virtually eradicated from livestock following lengthy and expensive control programs [70]. The Eastern Mediterranean that consists of 22 countries, including Iran is one of the most important endemic regions for brucellosis infection. Annually more than half a million incident cases of brucellosis are notiﬁed from countries in this region [10]. The annual incidence of brucellosis in Middle Eastern and Mediterra- nean regions varies between 1 and 78 cases per 100,000 populations[12,71,72]. This disease does not limited to Middle East and is prevalent in western parts of Asia, India, Southern European, and Latin American countries[70,73]. In general, according to hygiene world organization reporter prevalence of infection is varies widely from<0.01 to 200 per 100,000 population, so that in native areas of America 1 person in 100,000, in England 0.3 persons in 1 million, in German 0.03 persons in 100,000 and in rural areas of Greece 0.3 persons in 100,000 suffering from the disease[74e78]. Based on the report of the Ministry of Health, the incidence of brucellosis in Fig. 2.Distribution of brucellosis in different regions of Iran (The numbers are based upon the %).

Table 2

Status of brucellosis infection among included studies.

status No. of studies Point estimation^a 95% CI^U Asymptotic Test for heterogeneity

upper lower z-value p-value I² P-value

ﬁxed 34 0.000 0.000 0.001 4.111 <0.001 0.000 <0.994

random e 0.000 0.000 0.001 4.111 <0.001 e e

aRandom-effects modelU95% conﬁdence Interval.

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Fig. 3.Forest plot of meta-analysis on log incidence of brucellosis with 95% CI (Illustration of weighted relative frequency using random effects model for assessing pooled annually incidence rate of brucellosis).

Fig. 4.Inﬂuence plot for sensitivity analysis.

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Iran varies from 114/100,000 to 225/100,000 in highly endemic areas[19]. According to a study (2003), the average incidence of brucellosis in the Iranian population was 21 cases per 100,000 people, although this varied between 1.5 and 107.5 per 100,000 people in different regions of the country[79].

Unfortunately, despite the existence of high prevalence of brucellosis in Iran, there are no comprehensive and systematic data about the incidence of this infection. Therefore, we tried to done one exhaustive study on incidence of brucellosis in 18 years' period, from 1996 to 2014 in over of Iran country. Results of our research extracted from 34 articles indicated that incidence of brucellosis in investigated studies varies in different province, so that the lowest rate of incidence reported from Qom with 7.0/100000 and the highest rate was related to Kermanshah province with 276.42/

100000 people. We tried to compare our results with several studies in the countries of American, European and Asia. Some reports in the Middle East in 2002 showed that the countries with the highest incidence of human brucellosis are Saudi Arabia (32.8/

100,000), Iran (29.8/100,000), Palestine (21.5/100,000), Syria (21.0/

100,000), Jordan (20.4/100,000) and Oman (16.6/100,000). Bahrain and Cyprus have reported zero incidences[80]. According to annual reports in Egypt, Saudi Arabia, Oman, Jordan and Syrian Arab Re- public reported a combined annual total of more than 90,000 cases of human brucellosis[58]. Also in other countries there are several reports related to epidemiology of brucellosis. In Serbia, reported cases of this infectious disease decreased from 324 patients in 1991 to 2 patients in 2008 [81]. Moreover, in a study in Bosnia and Herzegovina it was revealed that brucellosis incidence was 33.4 per 100,000 people in 2008[82]. According to a study in Kuwait, the annual incidence has risen from 1.2 in 1976 to 69/100,000 in 1985 [83]. According to study carried out by Mantur et al. (2008) the incidence rate of human brucellosis in India was reported 8.5 cases per 100000 populations[84]. Zhang et al. (2014) showed nation- wide surveillance data indicated that the total prevalence rate of human brucellosis in China increased from 0.92/100,000 people in 2004 to 2.62/100,000 people in 2010. This data suggests that human brucellosis is an important public health problem in China [85]. In Turkey, the prevalence rate of the disease had risen to over 25.6 cases per 100,000 in 2004 year[86]. In European countries, human brucellosis has become uncommon, so that in Germany only 31 cases of disease reported in the years 2002 and 2003[87].

Our results indicated that the average incidence of brucellosis

was 100 cases per 100,000 individuals. Thisﬁnding is consistent with regional rates. A systematic review reported that the prevalence of brucellosis infection ranged from 0.73 to 149.54 per 100000 individuals per year in Middle Eastern countries. Our study also showed that based on sub-national studies, in Iran this rate varies from 7.00 to 276.42 per 100000 people in this 18 years period [88].

5. Conclusion

Brucellainfection remains an important public health issue in endemic areas such as Iran, and much remains to be done to reach the aim of controlling human and animal infection. According to the results of this study, annually incidence rate of brucellosis is in a high rate in some parts of Iran, and likely to rise; thus, measures should be taken to control the transmission pathway of infection from domestic animals and their products to human. In addition, the rapid identiﬁcation of sick animals and dispose of them as well as using advanced laboratory techniques for exact and fast diagnosis can be helpful in reducing the incidence and prevalence of infection. An incorporated approach to disease surveillance involving both human health and veterinary services would allow a better understanding of disease dynamics at the human-animal interface, as well as a more cost-effective utilization of resources.

Ethical approval Not required.

Funding No funding.

Authors' contribution

MS andSM contributed to the conception and design of the work; the acquisition, analysis, and interpretation of data for the work.FMJcontributed to data collection and interpretation of data for the work.RMcontributed to design of the work, data collection and ﬁnal approval of the version to be published. MSand FMJ contributed in data analysis, Drafting the work and revising it critically for important intellectual content.RMandSMcontributed in the revising the draft and agreement to be accountable for all aspects of the work in ensuring that questions related to the ac- curacy or integrity of any part of the work are appropriately investigated and resolved.

Conﬂict of interest

Authors declares that there are no conﬂict of interests in the present study.

Informed consent

All authors approved theﬁnal version of the manuscript.

Acknowledgement

The authors are greatly thankful to Saadat Pirouzi for help with the English language version of this paper. Also, we would like to thank the director and principal of Iran university of medical sciences for their constant encouragement and support of research for this study.

Fig. 5.Funnel plot of the relative frequencies (RFs) versus the standard errors of the Framingham risks in studies that evaluated the brucellosis in Iranian patients (with pseudo 95% conﬁdence intervals).

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