Global prevalence of human brucellosis: A systematic review and meta-analysis

doi:10.21203/rs.3.rs-4929733/v1

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Global prevalence of human brucellosis: A systematic review and meta-analysis

https://doi.org/10.21203/rs.3.rs-4929733/v1

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Background and aim: Human brucellosis caused by various Brucella species is a significant global health concern, particularly in livestock-dependent regions. The disease presents with non-specific symptoms like fever, fatigue, and joint pain, often leading to complications such as endocarditis and arthritis. Accurate diagnosis of this condition is challenging due to its diverse clinical manifestations and similarities to other febrile illnesses. This study aimed to provide a comprehensive synthesis of literature on the global prevalence of human brucellosis, providing updated insights and recommendations for improving diagnostic methods and public health strategies.

Materials and Methods: In this study, a systematic search of Web of Science and Scopus was performed to extract studies from January 2000 to December 2022 using keywords “Brucellosis”, “Brucella”, “prevalence of Brucella”, “prevalence of brucellosis”, “epidemiology of Brucella”, and “epidemiology of brucellosis”. Extracted data were than imported to HubMeta, duplicates were removed, and relevant studies (original articles/abstracts in English) were screened by reviewing titles, abstracts, and full texts. Cross-sectional and retrospective studies on brucellosis prevalence were included, while case reports with fewer than ten patients, clinical trials, and studies without clear sample sizes were excluded. Data were extracted into an Excel sheet and analyzed using the Meta Essentials tool to calculate pooled, gender-specific prevalence, and continent-specific prevalence with results visualized using forest plots.

Results: Sixty-nine studies with a sample size of 2,00,1236 were included in the review. The pooled prevalence of brucellosis was 15.49% (95% CI: 12.01–18.97), with the highest prevalence observed in Palestine (76%) and the lowest in Brazil (0.64%). The prevalence by continent was 16.65% in Asia, 16.28% in Africa, and 11.09% in America. The gender-specific prevalence was 19.11% in males and 13.97% in females.

Conclusion: This meta-analysis revealed significant regional and gender disparities in the prevalence of brucellosis, with high rates in Asia and Africa and a higher prevalence in males due to occupational exposure. However, limitations such as language bias, high study heterogeneity, and uneven study distribution across countries may affect the generalizability of the results. Standardized diagnostic methods and targeted public health interventions are essential to reduce the impact of brucellosis.

Brucella

epidemiology

zoonosis

public health

veterinary public health

brucellosis.

Human brucellosis caused by bacteria of the genus Brucella remains a critical global health issue, particularly in regions reliant on livestock. This zoonotic disease was formerly known as Malta fever, Mediterranean fever, Gibraltar fever, Cyprus fever, and Undulant fever [1]. Brucella has several identified species like B. melitensis (goats, sheep and camels), B. abortus (cows), B. suis (pigs), and B. Canis (dogs) and B. neotomae (rodents). Among several species identified in Brucella, B. melitensis is the most invasive species, causing more severe disease. On the other hand, B abortus is most widely distributed, but it is less pathogenic in both animals and humans. B. Suis is a serious pathogen in humans while B. Canis causes mild infection [2]. B. neotomae is also considered a zoonotic risk factor for infection in humans [3]. Common symptoms, such as fever, chills, loss of appetite, sweats, weakness, fatigue, joint, muscle, and back pain, and headache, may occur in patients. Long-term impacts can cause endocarditis, arthritis, epididymo-orchitis, meningitis, and encephalitis (4).

More than 170 countries and regions worldwide have reported human and animal brucellosis [5]. A total of 500,000 cases of human brucellosis are reported annually [6]. It is endemic in many countries, and its incidence varies widely from < 0.01 to > 200 per 100,000 [7]. The notification rate in the EU/EEA was 0.04 cases per 100,000 people. Greece has the highest notification rate (0.33 cases per 100,000 people) [8]. Brucellosis affects both genders; however, certain studies suggest high-risk factors among males, potentially due to occupational exposure related to farming, slaughterhouse, and animal product industries.[9]. However, gender differences in reported cases may also be influenced by social and cultural factors that affect access to healthcare and diagnostic services [9]. Accurate gender-specific data are essential for developing targeted public health interventions and improving disease management strategies.

The diagnosis of brucellosis remains challenging due to its diverse clinical manifestations, which can mimic other febrile illnesses such as malaria, typhoid fever, dengue fever, leptospirosis, rickettsial infections (e.g., Rocky Mountain Spotted Fever, typhus), Q fever, tuberculosis, endocarditis, and rheumatic fever. The Rose Bengal test (RBT), based on a slide agglutination test and the standard agglutination test (SAT) in tubes are the most common serological tests used for diagnosing B. abortus, B. melitensis, and B. suis infections, with the newly developed SAT miniaturized test, in areas where zoonosis is endemic [10, 11]. Blood culture is considered the gold standard for the diagnosis of brucellosis. Recent advancements in molecular diagnostics, such as real-time polymerase chain reaction (RT-PCR), are rapid, reliable, highly sensitive, and specific method for molecular diagnosis, but they depend on the availability of specific DNA in serum samples. Thus, a combination of different tests should be used for a definitive diagnosis. Usually, the SAT is used for screening, and the Coombs’ test or complement fixation test (CFT) is used as a confirmation test [12].

To support accurate control measures in host maintenance, recognizing the biology of Brucella infections and its species and patterns of transmission in wildlife, as well as between livestock and humans, is of particular importance [13]. The most rational approach for preventing human brucellosis is controlling and eliminating the infection in animals and pasteurizing milk [14]. Before implementing any control or eradication program, it is necessary to identify the Brucella species that infect animals, and the necessary interventions should be integrated into the One Health program [15].

Previous systematic reviews [16–18] on brucellosis have provided valuable insights into its epidemiology and diagnostic approaches. However, these reviews often face limitations, such as a narrow geographical focus [17] and small sample size [16]. This study aimed to synthesize the existing literature on the global prevalence of human brucellosis. This study seeks to provide a more comprehensive and accurate overview by incorporating a larger sample size and offering prevalence data based on gender and continent-pooled prevalence. Additionally, we include detailed discussions on diagnostic strategies and recommendations for improving public health interventions.

Ethics approval:

Ethics approval was not necessary for this study. This study was conducted according to the Preferred Reporting Items in Systematic Reviews and Meta-Analyses (PRISMA) guidelines [19].

Method of literature search

Complete and comprehensive searches were conducted in Web of Science and Scopus, from January 2000 to December 2022. In the search, the following keywords, including “Brucellosis”, “Brucella”, “prevalence of brucella”, “prevalence of brucellosis”, “epidemiology of brucella”, and “epidemiology of brucellosis” were used.

The extracted data were imported into HubMeta (https://hubmeta.com/) [20]. Thereafter, duplicated articles were removed, and the remaining studies were screened. The titles and abstracts of the articles were initially assessed. Articles that met the inclusion and exclusion criteria were subsequently subjected to a full-text review, which was also conducted in accordance with the same criteria.

Inclusion and exclusion criteria

All cross-sectional and retrospective studies reporting on the prevalence of brucellosis were included. However, case reports and case series with less than 10 patients (as the sample size) and clinical trial studies were excluded. In addition, studies without clearly defined sample sizes and prevalence estimates, case–control studies, and abstracts presented in conferences without full texts or texts with only institutional access were excluded from further processing.

Data Extraction and Statistical Analysis

In the present study, an Excel® data sheet (Microsoft Excel 2021) was designed. From all eligible studies, general (author name, country, enrolment time, published year, study design, sample size, gender, number of brucellosis positive patients, gender, diagnostic methods, isolated bacteria, and prevalence%) data were extracted. All data used in this study were analyzed using the Meta Essentials Excel sheet (Erasmus Research Institute of Management, Netherlands) [21], an Excel-based tool for meta-analysis. A meta-analysis was conducted to calculate the pooled prevalence of brucellosis at 95% confidence interval. Additionally, the continent-specific and gender-specific prevalence of brucellosis were also calculated at 95% confidence interval. The results were graphically represented using forest plots.

In total, 4,390 records were identified through the databases. After removing 482 duplicate records, 3,908 records were screened. From these, 3,635 records were excluded based on title and abstract, leaving 273 reports assessed for full-text eligibility. Of these, 204 full-text articles were excluded based on exclusion criteria, resulting in 69 studies included in this review with a sample size of 2,00,1236. A flow chart of the selection process is presented in Figure 1.

Pooled prevalence of human brucellosis

The prevalence of brucellosis in all eligible studies (n = 69) and the forest plot of study-wise brucellosis prevalence are illustrated in Table 1 [22-90] and Figure 2, respectively. The minimum prevalence (0.64%; 95% CI: -2.52–3.80) of brucellosis was reported by Clazer et al. (41) in Brazil, whereas the maximum prevalence (76%; 95% CI: 73.68–78.32) was reported by Alzuheir et al. [60] in Palestine. Based on the results of the random-effects model approach (Figure 2), the pooled estimate of the prevalence of brucellosis was 15.49% (95% CI: 12.01–18.97; heterogeneity I² index: 99.73%).

Pooled prevalence of brucellosis according to continent

Figure 3 illustrates the pooled prevalence of brucellosis stratified by continent. The analysis encompassed studies from Asia (38 studies), Africa (24 studies), America (6 studies), and Europe (1 study), with the Americas representing both North and South America.

The pooled prevalence of brucellosis was as follows: 16.65% (95% CI: 7.36, 25.95; heterogeneity I² index: 99.71%) in Asia, 16.28% (95% CI: 9.06, 23.49; heterogeneity I² index: 99.35%) in Africa, and 11.09% (95% CI: -5.54, 27.72; heterogeneity I² index: 97.51%) in America. In Asia the highest prevalence of brucellosis was recorded in Palestine 76.00% (95% CI: 67.53, 84.47). In Africa, Morocco exhibited the highest prevalence of 33.20% (95% CI: 30.65, 35.75), whereas the highest prevalence in America was 18.10% in Mexico. (95% CI: 13.93, 22.27).

Pooled prevalence of brucellosis according to gender

Figure 4 presents the pooled prevalence of brucellosis stratified by gender. The analysis included multiple studies on both males and females. For males, the pooled prevalence of brucellosis was 19.11% (95% CI: 10.38, 27.84; heterogeneity I² index: 98.99%). The highest prevalence among males was reported by Getahun et al. [77] with a rate of 82.62% (95% CI: 78.65, 86.59). Other studies also showed significant prevalence rates, such as Almashhadany et al [33] with 46.95% (95% CI: 39.25, 54.65) and Rahman et al. [70], with 32.14% (95% CI: 28.98, 35.30). For female, the pooled prevalence of brucellosis was 13.97% (95% CI: 8.00, 19.94; heterogeneity I² index: 97.39%). The highest prevalence among females was reported by Almashhadany et al. [33]. with a rate of 48.12% (95% CI: 39.55, 56.69). Other notable prevalence rates included Rahman et al. [70] with 29.69% (95% CI: 26.19, 33.19) and Kiambi et al. [50] with 11.11% (95% CI: 6.97, 15.25).

The aim of this systematic review and meta-analysis was to provide a comprehensive and updated assessment of the prevalence of brucellosis globally, addressing the significant gaps identified in previous studies; unlike earlier research, which often suffered from limited geographic scope [17, 91] and small sample sizes [16]. This study aggregated data from 69 diverse studies with a total sample size of over 2 million individuals, thereby providing a more robust and generalized prevalence estimate. This study highlights variations in diagnostic methods and control measures, thereby providing valuable insights into how these factors influence prevalence estimates.

High and Low Prevalence by Country and Continent

This study provides a comprehensive view of the prevalence of conditions across various continents, revealing notable regional differences. In Asia, prevalence rates vary significantly, from 3.69% in China [34, 75] to 76% in Palestine [38]. This wide range may reflect differences in disease burden, healthcare access, and reporting practices. The lower prevalence in China might indicate more effective public health interventions and diagnostic practices. In contrast, the high prevalence in countries like Palestine, Georgia (41%) [29], and Mongolia (32.82%) [49, 81] suggests that local factors such as environmental or genetic predispositions could influence the prevalence.

Similarly, Africa exhibits considerable variability in prevalence rates. Morocco has the highest rate at 33.2% [76], while Cameroon has the lowest at 0.98% [62]. This high prevalence in countries like Morocco and Sudan could be linked to socioeconomic conditions, healthcare infrastructure, or population density. Conversely, lower rates in Cameroon and Nigeria may result from under-reporting, different diagnostic criteria, or lower actual disease burden.

In America, prevalence rates are higher in Mexico and the United States than in Brazil. Mexico’s prevalence of 18.1% [64] contrasts with Brazil’s 4.61% [25, 30, 56, 89], suggesting regional differences in factors such as healthcare systems, public health policies, and socioeconomic conditions. These differences highlight the need for region-specific health strategies and potentially more tailored interventions.

Europe’s data are limited to Portugal, which has a prevalence rate of 7.2% [36]. The lack of additional data from other European countries means that we cannot draw broader conclusions on prevalence in Europe as a whole. However, available data for Portugal suggest a prevalence rate that is moderate compared with other regions.

Overall, the data revealed substantial differences in prevalence rates across continents and countries. The high I² values in the meta-analysis indicate significant heterogeneity, suggesting that regional factors play a crucial role in these variations. Understanding these regional differences is essential for developing targeted public health strategies and interventions to manage and prevent disease.

Gender-Wise Prevalence

The analysis of the prevalence of brucellosis according to gender provides significant insights into the epidemiology of this infectious disease. For male, the pooled prevalence was notably high at 19.11%, with a very high heterogeneity (I² index: 98.99%), suggesting considerable variation among the included studies. The strikingly high prevalence rate of 82.62% reported by Getahun et al. [77] compared with other studies, reported such as 9.5% by Almashhadany et al. [33] and 2% by Rahman et al. [70], highlights the potential impact of regional differences or methodological variations. In contrast, the pooled prevalence of females was lower at 13.97%, although it still exhibited high heterogeneity (I² index: 97.39%). Almashhadany et al. [33] reported the highest prevalence among female (48.12%, indicating significant variability that might reflect differences in exposure risk, healthcare access, and reporting practices across studies. The differences in prevalence rates between genders and across studies suggest that the risk factors and transmission dynamics of brucellosis may vary by gender and geographic region.

These findings highlight the importance of considering both gender and regional factors when assessing the prevalence of brucellosis. The high heterogeneity observed in both male and female prevalence rates suggests that brucellosis is influenced by a complex interplay of factors, including environmental, socioeconomic, and diagnostic variables. Future research should address these discrepancies and provide more uniform data to better understand the epidemiology of brucellosis and develop targeted prevention and control measures.

Transmission and Control Measures

The transmission dynamics of brucellosis provide critical insights into the propagation of this zoonotic disease propagates among populations. Brucellosis is often transmitted to humans through direct contact with livestock. In regions where unpasteurized dairy consumption is common, such as in some parts of Africa and Asia, the risk of brucellosis and its prevalence could be notably higher [92, 93]. This underscores the importance of implementing pasteurization practices on a large scale in dairies and public health education to lower the transmission rate of dairy products.

In addition to dairy consumption, occupational exposure plays a crucial role in brucellosis transmission. Individuals working in veterinary fields, livestock management, and abattoirs are at higher risk due to frequent contact with potentially infected animals or secretions (94). This occupational risk is reflected by the higher prevalence rates observed in males, who are more likely to be employed in high-risk environments.

Furthermore, the high heterogeneity in prevalence rates observed in selective studies indicates the influence of local practices, animal husbandry conditions, and variations in diagnostic and reporting standards. Overall, a comprehensive approach that includes improving animal health practices, enforcing pasteurization, and protecting high-risk occupational groups is vital for reducing the transmission of brucellosis and its impact on public health (93, 94).

Diagnostic tests

Table 1 illustrates the variation in the prevalence rates of brucella infections among different diagnostic tests, which is influenced by their sensitivity and specificity. Rapid tests, such as the Rose Bengal plate test (RBPT) and the Rose Bengal test (RBT), are known for their high sensitivity but exhibit a broad range of prevalence rates (0.98–54.53%), which can be attributed to the potential for false-positive results due to cross-reactivity. Similarly, the enzyme-linked immunosorbent assay (ELISA) shows a wide prevalence range (0.64–76%), reflecting its high sensitivity and ability to detect various stages of infection, although it also exhibits variability in accuracy. More specific tests, such as the complement fixation fest (CFT), generally have lower prevalence rates (1.2–4.68%) due to their high specificity, which minimizes false-positives but may result in some infections being missed.

This meta-analysis highlights substantial regional and gender disparities in the prevalence of brucellosis, with particularly high rates in Asia and Africa. The elevated prevalence in countries such as Palestine and Morocco underscore a critical public health issue linked to extensive livestock farming and occupational risks. The observed higher prevalence in males reflects increased exposure in farming, slaughterhouse, and animal product industries.

The variability in diagnostic methods significantly influences reported prevalence rates, emphasizing the need for consistent and advanced diagnostic techniques to accurately assess and manage brucellosis. To address these challenges, targeted public health interventions, including enhanced diagnostic capabilities, vaccination programs, and comprehensive awareness campaigns, are needed. Such measures are essential to mitigate the impact of brucellosis and improve disease management, particularly in the most affected regions.

Limitations

This review is subject to several limitations. First, the selection of studies was restricted to those published in English, which may have excluded relevant research published in other languages and introduced potential language bias. Second, the high heterogeneity across studies necessitated the use of a random-effects model, which may have affected the precision of the pooled estimates. Additionally, our findings have uneven distribution of studies across different countries, with insufficient data from certain regions potentially affecting the generalizability of the results. Future research should aim to include studies from a broader range of languages and consider conducting cross-sectional or retrospective studies in countries that are currently underrepresented to address the uneven distribution of data.

CS: Cross-sectional, M: Male, F: Female, ELISA: Enzyme-linked immunosorbent assay, RBPT: Rose bengal plate test, EIA: Rnzyme immunoassay, STAT: Standard tube agglutination test, RBT: Rose bengal test, 2-ME: 2-mercaptoethanol, PAT: Plate agglutination test, WT: Wright test, IIF: Indirect immunofluorescence, FBAT: Febrile antigen Brucella agglutination test, CFT: Complement fixation test, RT-PCR: Real-time polymerase chain reaction , SPAT: Standard plate agglutination Test, CRAT: Commercial rapid agglutination test, BcT: Brucellacapt test, SIAA: Single-Step immunocapture agglutination assay, qPCR: Quantitative polymerase chain reaction, SAT: Slide agglutination test, MAT: Microagglutination Test

Ethics Approval and Consent to Participate

Not applicable

Consent for publication

Not applicable

Availability of data and materials

The original data and materials related to this study are available in the article. For additional inquiries, please contact the corresponding author.

Competing Interests

The author declares that there are no competing interests.

Funding

The author received no funding for this study.

Author contributions
RS designed the study, performed paper searching, selection, extraction of data, conducted results interpretation, and drafted the manuscript. RS also reviewed and approved the final manuscript.

Acknowledgement

Not applicable

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Global prevalence of human brucellosis: A systematic review and meta-analysis

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Discussion

High and Low Prevalence by Country and Continent

Gender-Wise Prevalence

Transmission and Control Measures

Diagnostic tests

Conclusion

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