https://orcid.org/0000-0003-2534-4953
Abstract
Camel brucellosis is a major public health concern in Sudan; however, there is no overall estimation of the prevalence of camel brucellosis in Sudan. Following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, this study aimed to perform a meta-analysis of 30 eligible studies published before December 31, 2022, with a total of 70059 dromedary camels, to estimate the pooled prevalence of camel brucellosis and its risk factors in Sudan. The random effect model was used for the final analysis due to the significantly high heterogeneity among the included studies, and the results showed that the overall pooled prevalence of camel brucellosis was 17%, with a confidence interval (CI) of 12%–21%. The prevalence was higher in males than females (54% vs. 46%) and in adults than youngling (77% vs. 23%). The prevalence also varied by region, with central and northern Sudan having the highest prevalence (24%), compared to other regions of Sudan. Moreover, the prevalence of camel brucellosis appeared to be decreasing over time. The current study concluded that camel brucellosis infection is still endemic in many areas of Sudan, with the disease being especially prevalent in central and northern Sudan. Thus, this study provides valuable information for the prevention and control of camel brucellosis in Sudan. However, the significant heterogeneity among the included studies should be taken into account when interpreting these results. Finally, to provide adequate information, research must be updated, and more research must be conducted in many regions of Sudan.
1. Introduction
Brucellosis is a contagious zoonotic bacterial disease caused by various Brucella species, and it affects most warm-blooded animals (Seleem et al. Citation2010). However, the most vulnerable animals to brucellosis are cattle, small ruminants, camels, pigs, and dogs (Pappas et al. Citation2006; Seleem et al. Citation2010). Infected animals usually show unique clinical manifestations, such as abortion in females and orchitis that lead to infertility in males (Megid et al. Citation2010; Dean et al. Citation2012). Zoonotic brucellosis occurs when people are in contact with infected animals or animal products that are contaminated with bacteria, and it has been reported in almost all countries worldwide with a pooled prevalence of 15.27% (Pappas et al. Citation2006; Khoshnood et al. Citation2022). In general, brucellosis is considered one of the major public health concerns, especially in developing settings (e.g. countries of Sub-Saharan Africa) where it remains endemic (Suresh et al. Citation2022).
In Sudan, brucellosis has a long history (Dafaalla Citation1962; Erwa Citation1966). The first human case was diagnosed in 1904. In the succeeding years, studies focused on extensive monitoring of the disease to identify its transmission routes and to find infected humans and animals. In 1943, Brucella abortus was first diagnosed and isolated from some dairy cows imported from the United States (Williams Citation1939; Erwa Citation1966). The disease was diagnosed in a local cow breed for the first time from aborted cows in Juba in 1962 (Dafaalla Citation1962). Following these early detections, several brucellosis outbreaks occurred in cattle, goats, sheep, camel, and horses all over the country, so much so that now the disease is endemic in Sudan with varying prevalence in different animals (El-Ansary et al. Citation2001; Musa Citation2004; Mokhtar et al. Citation2007; Mahmoud and Atif Citation2012).
In camels, brucellosis is mainly caused by B. abortus and B. melitensis as a result of direct or indirect contact with the primary hosts of these two Brucella species (Abbas and Agab Citation2002; Sprague et al. Citation2012). In Sudan, camel brucellosis draws special attention because camels are considered profitable animals. They can survive in harsh environments and graze in low-productive pastures and relatively produce high amounts of milk and meat (Abdurahman Citation2004; Blackwell Citation2010). Moreover, camel food products are very valuable resources of nutrition for nomads and populations in arid regions in Sudan, especially during the past few years due to climate changes (Ahmed SM Citation2020).
Several epidemiological studies have investigated the seroprevalence and risk factors of brucellosis in camels generating scientific data/information that helped in developing epidemiological knowledge and allowed for the implementation of informed-control and prevention strategies. This led to significant progress in the control of brucellosis during the last decades in Sudan. However, there is still an increasing concern about the financial losses associated with the disease due to its zoonotic nature. Therefore, there is a need for a meta-analysis to report the overall prevalence of camel brucellosis at the national level to advance the effort of control. The current study aimed to systematically review the available literature reporting camel brucellosis and perform a meta-analysis to find the pooled prevalence of camel brucellosis and its associated risk factors in Sudan.
2. Materials and methods
2.1. Data items, information sources, and search strategy
This meta-analysis followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (Page et al. Citation2021), and the protocol has been registered prospectively in the International Prospective Register of Systematic Reviews (No. CRD42021256122).
The current study’s main finding was the prevalence of camel brucellosis in Sudan, which was determined by direct reports from individual studies, and the results were interpreted by comparing the percentages of camels that tested positive for brucellosis to the total camel population studied. Separate searches were conducted by two investigators (Abdullah Mohammed and Musa Ahmed) in research databases () from their inception to December 31, 2022, for studies on camel brucellosis published in English and/or Arabic. Using the research strategy, devised using Boolean search terms (AND, OR, NOT), the final search strategy of the current study employed titles and abstracts related to ((brucellosis) OR (Brucella abortus) OR (Brucella melitensis)) AND ((prevalence) OR (epidemiology) OR (frequency)) OR (risk factors)) AND ((dromedary camels) OR (Camelus dromedarius) OR (Arabian camels) OR (one-humped camels)) AND (Sudan)).
Table 1. Databases searched and number of hits.
2.2. Eligibility criteria
The following criteria were used to determine eligibility for the current study: (1) all observational studies; (2) published in Arabic or English; (3) conducted on dromedary camels (camel dromedarius) in Sudan; (4) reported the prevalence of brucellosis; and (5) positive cases of brucellosis must be detected using the standards’ serological diagnostic methods. Studies were not eligible for this study if they did not provide sufficient information on the sample size, sampling location, or sampling period, as these factors may affect the representativeness and quality of the data. In addition, studies were excluded from this study if they were reviews, letters, or editorials, or if the full text was not available and had been requested from the correspondent author(s) through email but no feedback was received after 3 weeks.
2.3. Study selection process and risk of bias assessment
The selection process of studies was done based on the inclusion and exclusion criteria, which started with the primary screening of the all-electronic databases to identify the eligible studies and retrieve them. Thereafter, these studies were exported to version X9.3.3 of the EndNote citation manager to identify duplicates and remove them. Following that, two investigators (Abdullah Mohammed and Musa Ahmed) independently screened the titles and abstracts of the retrieved records for eligibility based on the inclusion and exclusion criteria. Any differences in the study selection process were resolved by discussion and consensus, or by consulting a third investigator (Ahmed Osman Ahmed) if needed. The inter-rater agreement between the two investigators was measured using Cohen’s Kappa statistic, which ranges from 0 (no agreement) to 1 (perfect agreement). A kappa value of 0.61–0.80 was considered substantial agreement, and a value of 0.81–1.00 was considered almost perfect agreement (Gwet Citation2008). The full texts of the potentially relevant articles were obtained and assessed for eligibility by the same investigators using the Joanna Briggs Institute quality assessment tools checklist (Jordan et al. Citation2019). The PRISMA statement flow diagram (Page et al. Citation2021) was used to depict the entire selection process ().
Figure 1. Flow diagram of the studies included in this meta-analysis.
2.4. Data collection process
After completing the study selection process, the relevant data was extracted using a Microsoft Word 2016 data extraction template.
For any study that did not report the information needed to meet the above-mentioned eligibility criteria, the primary investigator (Abdullah Mohammed) contacted the corresponding author (via email) to obtain the original data; further, if the primary investigator failed to obtain the missing information or it was not obtained after 2 weeks, the study or studies with the missing information were removed. The extraction template includes the following information: the author’s name and publication year, study period, diagnostic method, state, geographical location (based on state names), type of brucellosis (B. abortus or/and B. melitensis), sample size, the prevalence of camel brucellosis (overall and in males and females) (), and risk factors for camel brucellosis (). The accuracy of the data extraction process was confirmed by comparing the extraction results of two authors (Abdullah Mohammed and Musa Ahmed) who extracted the data independently from a randomly selected set of papers (30% of the total).
Table 2. Main characteristics of studies included in the meta-analysis.
2.5. Synthesis methods
The current study’s data were analyzed using STATA software version 16.0 (Stata Corp LLC, 77845 Texas, United States). Furthermore, for the meta-analysis results, the statistical significance level was set at p < 0.05. The degree of inconsistency (I2), which is expressed as a percentage and ranges from 0% to 100%, was used to assess heterogeneity among the included studies. To quantify the I2 result, the current study follows the recommendation of Higgins et al. (Citation2003), which defined heterogeneity as low, medium, and high for I2 values of 25%, 50%, and 75%, respectively. This study’s results were calculated using two statistical measurements: effect size with a 95% confidence interval (CI) and standard error (SE). The effect size of this study was calculated using the binomial distribution and the prevalence of brucellosis (proportion). Meanwhile, using the SE formula, the standard error of the proportion was calculated using the sample size (n) and the proportion of brucellosis positive cases in the overall population (p): SE = sqrt [p (1-p)/n].
The results of each individual study, as well as the pooled results of all included studies, were presented as forest plots in the final meta-analysis model [reported as effect size (prevalence) with a 95% CI]. To check for potential publication bias, the visual symmetry of the funnel plot and the result of the regression-based Egger test (Egger’s test) were used; however, unlike the other statistical tests reported here, Egger’s test was considered significant if the P values were less than 0.10.
To investigate the possible relationship between study variables (study year(s), sample size, diagnostic method, type of brucellosis, and study region) and the prevalence of camel brucellosis, a meta-regression test (univariate and multivariate regression) was performed. Meanwhile, sensitivity and subgroup analyses were carried out to assess potential heterogeneity among the included studies and potential sources of bias.
Finally, the results of this study were presented using a narrative synthesis, followed by the full meta-analysis chart, in accordance with the PRISMA guidelines.
3. Results
3.1. Study selection
depicts the entire study selection process, in which 524 scientific articles were identified from major electronic databases and other relevant sources. Due to duplication, 170 articles were immediately removed, while 354 studies were retained for further critical evaluation. As a result, 307 studies were excluded after being meticulously screened based on their titles and abstracts. However, 17 of the remaining 47 articles were rejected due to inconsistencies with the current study eligibility criteria. Finally, only 30 of the 524 initial studies met the eligibility criteria and were included in the systematic review and meta-analysis (see ).
Figure 2. Distribution of the number of studies on the prevalence of camel brucellosis in Sudan over time.
3.2. Study characteristics
and show the main characteristics of the studies included in this comprehensive study. A total of 30 studies, involving a total of 70059 dromedary camels, were included in the qualitative and quantitative analysis. All the included studies reported on the overall prevalence of camel brucellosis in Sudan. Eleven studies demonstrated an association between gender and camel brucellosis. In addition, other risk factors, namely, camel age, the purpose of raising the camel, the grazing system, and the previous history of abortion, were reported in 9, 4, 2, and 1 studies, respectively.
Table 3. Risk factors of camel brucellosis in Sudan.
Meanwhile, from all available serological diagnostic tests for brucella, only four tests were mentioned in the included studies: (1) the rose bengal plate test (RBPT) – 27 times; (2) the modified rose bengal plate test (mRBPT) – 3 times; (3) the enzyme-linked immunosorbent assay test (ELISA) – 3 times; and (4) the serum agglutination test (SAT) – 1 time.
In the current study, only two brucella species were found in dromedary camels in Sudan (B. abortus and B. melitensis); thus, the disease in Sudan has two types: one caused by B. abortus alone (4 studies) and the other by the two species combined (26 studies). Furthermore, the result showed that camel brucellosis was distributed in almost all states, and specifically, the geographical distributions of included studies revealed that eastern Sudan (11 studies) was the most frequently studied area, followed by western Sudan (6 studies), central Sudan (3 studies), and only one study from northern and southern Sudan. Additionally, it can be noted that eight studies were from nationwide surveys.
3.3. Results of synthesis
In the thirty included studies, the current study discovered a wide range of camel brucellosis prevalence in Sudan. Whereby, the lowest prevalence of camel brucellosis (3.6%) was reported in a national-wide study (Abbas et al. Citation1987), whereas the highest prevalence (51.2%) was reported in a study done in Tambool city, Gezira State (Abdel-Aziz et al. Citation2014) ().
Furthermore, the heterogeneity across the included studies in the current meta-analysis study was significantly high (with P 0.0001; I2 = 97.74%); thus, the random effect model (REML) was used for the final analysis, and the pooled prevalence of camel brucellosis in Sudan was found to be 17% (CI: 12%–21%) (see ).
Figure 3. Forest plot (random-effects model) for the pooled prevalence of camel brucellosis in Sudan.
3.4. Subgroup analysis
Given the current study’s high heterogeneity, a subgroup analysis was performed to determine the effect of gender, age, brucella species, study region, study years, camel purpose, grazing system, and previous history of abortion on the pooled prevalence of camel brucellosis (). Using the aforementioned risk factors, the findings of this study revealed that the pooled prevalence of camel brucellosis in Sudan was higher in males (46%) ( and ). Additionally, the adult camel (age more than 4 years) had a higher pooled prevalence of brucellosis (77%) in comparison with young camels (age less than 4 years) (23%) ( and ); also, central Sudan and northern Sudan, those two regions, have the highest pooled prevalence of camel brucellosis (24%), compared with other regions of Sudan ( and ). Furthermore, the prevalence of camel brucellosis seems to have decreased over time, from 23% in the time period before 2000 to 18% in the time period after 2010 ().
Figure 4. Forest plot (random-effects model) for the pooled prevalence of brucellosis in males and females camel Sudan.
Figure 5. Forest plot (random-effects model) for the pooled prevalence of camel brucellosis in different age groups in Sudan.
Figure 6. The geographical distribution of camel brucellosis pooled prevalence in Sudan by regions (blue for the northern region, red for the eastern region, purple for the central region, yellow for the southern region, and orange for the western region).
Figure 7. Correlation of prevalence of Brucellosis in dromedary camel based on linear model regression; (A) sample size, (B) year of study, (c) diagnostic method, (D), brucellosis species, and (E) study region.
Figure 8. Funnel plot for assessing publication bias in the Pool prevalence of camel brucellosis in Sudan.
Table 4. Subgroup analysis of the effect of gender, age, Brucella species, study region, study years, camel rising purpose, grazing system, and previous history of abortion on the pooled prevalence of camel brucellosis (based on a random-effects model).
In addition, it is very important to know that, in this study, camels raised for meat production or/and milk production had a higher pooled prevalence of brucellosis compared with camels raised for racing purposes, and as expected, camels living in the outdoor grazing system had a higher chance to have brucellosis compared with camels living in the indoor system ().
3.5. Meta-regression and sensitivity analysis
A meta-regression test (both univariate and multivariate regression) was performed in addition to the main analysis to investigate the possible relationship between study variables (study year/s, sample size, diagnostic method, type of brucellosis, and study region) and the prevalence of camel brucellosis (). Interestingly, all those examined variables didn’t show any statistically significant association (), so we can conclude that these study variables did not affect the current study heterogeneity. In addition, for better clarification, a sensitivity analysis was performed to identify potential sources of heterogeneity among the included studies. This was accomplished by sequentially excluding studies from the analysis model; however, the results revealed no significant difference in the analysis model. As a result, it is possible to conclude that the current study’s meta-analysis finding was stable. Finally, two methods were used to assess publication bias: a funnel plot (), which was symmetric, and the regression-based Egger test (Egger’s test), which was statistically insignificant (p = 0.206); from that, it can be concluded that there is no publication bias in this study.
Table 5. Heterogeneity-related variables for the pooled prevalence of camel brucellosis in the current meta-analysis (based on meta-regression).
4. Discussion
Camel brucellosis is a contagious zoonotic disease characterized by genital organ and fetal membrane inflammation, abortion in late pregnancy with retained placenta, sterility, and the formation of lesions primarily in the lymphatic system and joints. In low-income countries such as Sudan, the economic and public health impact of brucellosis remains a source of concern. The disease is a serious threat to international animal trade and a barrier to free animal movement. Furthermore, the disease causes significant economic losses due to abortion or breeding failure in the affected animal population, decreased milk production, and human brucellosis, which reduces the work capacity of people due to the sickness (Robinson Citation2003; Roth et al. Citation2003).
The purpose of the current study was to systematically review the available literature reporting camel brucellosis in Sudan and perform a meta-analysis to find the pooled prevalence of camel brucellosis and its risk factors in Sudan. Thus, the results of the current study contribute to the limited knowledge of camel brucellosis and also have great significance for infertility program coordinators and policymakers as they design and implement effective strategies for preventing and managing the disease. Also, the study data will be used as a baseline for other researchers who want to investigate further findings in this area.
In the current review, the national prevalence of camel brucellosis in Sudan for all methods revealed was 17% (), this pooled prevalence is relatively lower compared with reports from Nigeria (20.9%) (Akinyemi et al. Citation2022), and fresh milk samples from the Middle East countries (24%) (Abedi et al. Citation2020), meanwhile, the pooled prevalence of camel brucellosis in this study was higher than the prevalences reported from some African countries (Dadar et al. Citation2022); Niger (0.76%), Ethiopia (2.84%), Somalia (0.97%), Somaliland (3.52%), Kenya (8.29%), Libya (2.64%), Egypt (11.93), and Asian countries (Dadar et al. Citation2022); Saudi Arabia (13.32%), Kuwait (10.93%), United Arab Emirates (4.98%), Oman (0.34%), Yemen (3.02%), Jordan (12.25%), Iran (5.75%), and Iraq (5.2%).
All the above indicates that worldwide, Sudan has the second-highest pooled seroprevalence of camel brucellosis, which may raise some serious questions about the epidemiology of the disease and the efficiency of the veterinary system in the country to respond to the disease. Therefore, it seems that camel brucellosis remains a neglected disease with low attention from veterinary and health authorities in Sudan, and taking into account the importance of Sudan as a country that exports live camels and camel meat to neighboring countries, especially Egypt and the Arab Gulf countries (Younan et al. Citation2016; Abedi et al. Citation2020; El-Diasty et al. Citation2022), we thought that there was an urgent need for collaborative efforts to be made in the field of camel brucellosis control and eradication.
The present comprehensive study checked some risk factors of camel brucellosis in Sudan, and the result showed that camel gender, camel age, the purpose of raising the camel, the camel grazing system, study region, and study year/s have a significant association with the prevalence of camel brucellosis in Sudan. As shown in and , males were more likely than females to have brucellosis (54% vs. 46%). This result is in contrast with the available evidence from the following studies: a study on the pooled prevalence of camel brucellosis in 20 countries (Dadar et al. Citation2022), a study from Qatar (Alhussain et al. Citation2022), and a study from Ethiopia (Tadesse Citation2016).
This discrepancy can be explained by the fact that most of the studies included in this study were conducted in veterinary quarries for animals destined for export, and in these quarries, as a result of the laws of the country (El Dirani Citation2009), most of the animals were males; hence, it makes sense that the odds of brucellosis are greater in males in comparison to females.
In addition, as expected, the adult camels had a higher pooled prevalence of brucellosis compared with young camels (77% vs. 23%) ( and ). A similar trend was observed in findings from studies from, Kenya (Hughes and Anderson Citation2020), Ethiopia (Tadesse Citation2016), Qatar (Alhussain et al. Citation2022), and a study on 20 African and Asian countries (Dadar et al. Citation2022).
Additionally, it is important to note that central Sudan and northern Sudan have the highest pooled prevalence of camel brucellosis (24%), compared with other regions of Sudan. This indicates that these areas should be given special attention to find out the reason for the high prevalence of the disease in these areas and to help reduce the prevalence of the disease locally and at the national level.
Furthermore, the prevalence of camel brucellosis seems to have decreased over time, falling from 23% before 2000 to 18% after 2010. The use of control measures such as vaccination and control programs may explain why disease prevalence appears to have decreased in Sudan over time (Abdalla et al. Citation2021). However, more studies are needed to confirm these hypotheses and evaluate the effectiveness and feasibility of these interventions in different settings. Moreover, this is a good indicator of the low prevalence of camel brucellosis in Sudan, but there is still a need to increase efforts to reach a prevalence lower than the global prevalence (9.23%) (Dadar et al. Citation2022).
Finally, it is very important to know that, in this review study, camels raised for meat production or/and milk production had a higher pooled prevalence of brucellosis compared with camels raised for racing purposes, and as expected, camels living in the outdoor grazing system had a higher chance to have brucellosis compared with camels living in the indoor system.
Regardless of the seriousness of camel brucellosis in Sudan as concluded in this study, there is currently no data available about the disease’s direct and indirect economic impact on the country’s camel production sector; therefore, work needs to be done to fill the gap in this area. We thought that estimating the national prevalence of camel brucellosis was an important step in designing nationwide veterinary health responses to the disease.
Furthermore, we recommend that policymakers and governments collaborate and take immediate action to implement a national-wide epidemiological program to clarify the design of regional strategies and to guide the development of prevention and eradication programs during and after the COVID-19 pandemic.
The current study employed extensive and thorough search strategies, including both published and unpublished literature in Arabic and English. Furthermore, the current study evaluated the methodological quality of the individual studies using a standardized quality assessment tool. All of the above are considered strengths for the current study.
The present comprehensive review study has some limitations, in light of which its findings should be viewed. In this study, we searched for studies that only report seroprevalence of camel brucellosis; however, it is important to know that serological methods are tools in disease surveillance, and seropositivity may not reflect the current infection status or transmissibility of the pathogen.
The lack of data on camel breed, husbandry practices, herd size, and characterization, camel owners’ knowledge and practices against brucellosis, and other potential risk factors in some studies, as well as the relatively small sample size of some studies, are considered limitations of this study and may raise questions about their representativeness. Furthermore, the presence of significant heterogeneity among the included studies, as well as a lack of published research on camel brucellosis in northern and southern Sudan, should be considered when interpreting these findings. Despite these limitations, the current review provides a starting point for further research aimed at quantifying the risk of camel brucellosis in Sudan.
5. Conclusion
This systematic review and meta-analysis found that camel brucellosis infection is still endemic in many areas of Sudan, with the disease being especially prevalent in central and northern Sudan, and that males and adults were more susceptible to infection than females and young animals. The pooled prevalence of camel brucellosis, on the other hand, has decreased over time. The presence of significant heterogeneity among the included studies, as well as a lack of published research on camel brucellosis in northern and southern Sudan, should be considered when interpreting these findings. To provide adequate information, research must be updated, and more research must be conducted in many regions of Sudan.
Author contributions
Abdullah Mohammed, Musa AHMED, Ahmed Osman Ahmed, Suad HAMAD, and Sadam YOUSOF, conceived and designed the review. Abdullah Mohammed, Musa Ahmed, and Ahmed Osman Ahmed carried out the draft of the manuscript. Abdullah Mohammed is the guarantor of the review. Abdullah Mohammed, Musa AHMED, Ahmed Osman, Suad HAMAD, Sadam YOUSOF, Nasir Ibrahim, and Yassir SHUAIB developed the search strings. Abdullah Mohammed and Musa AHMED screened and selected studies. Abdullah Mohammed and Musa AHMED extracted the data. Abdullah Mohammed and Musa AHMED evaluated the quality of the studies Abdullah Mohammed, and Musa Ahmed carried out analysis and interpretation. Abdullah Mohammed, Musa AHMED, Ahmed Osman Ahmed, Suad HAMAD, Sadam YOUSOF, Nasir Ibrahim, and Yassir SHUAIB rigorously reviewed the manuscript.
Availability of data and material
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Acknowledgements
The authors would like to thank Dr. Ibrahim M. Yousif, a lecturer at the University of Bahri, who was instrumental in drawing the geographical map distribution of the pooled prevalence of camel brucellosis in Sudan.
Disclosure statement
All authors declare that there exist no commercial or financial relationships that could, in any way, lead to a potential conflict of interest.
Additional information
Funding
References
- Abbas B, Agab H. 2002. A review of camel brucellosis. Prev Vet Med. 55(1):47–56. doi:10.1016/s0167-5877(02)00055-7.
- Abbas B, el Zubeir AE, Yassin TT. 1987. Survey for certain zoonotic diseases in camels in Sudan. Rev Elev Med Vet Pays Trop. 40(3):231–233.
- Abdalla AA, Mursi D, Abdalla MA. 2021. Serological diagnosis and molecular detection of Brucella species in Camels in West Kurdufan state, Sudan. Sudan J Sci Technol. 22(1):19–27.
- Abdel-Aziz BE, Elbasheir HM, Altigani MA, Al-Hassan SF. 2014. A survey on some dromedary camel diseases at Tumbool slaughterhouse, Gezira State, Sudan. Bull Anim Health Prod Africa. 62(4):397–403.
- Abdellah IEM. 2021. Serological survey of brucellosis in camels (Camelus dromedarius) in Suakin Quarantine-Sudan. Khartoum, Sudan: Sudan University of Science and Technology;
- Abdelnassir TA, ELsanousi E, Khogali M. 2020. Serological study of camel brucellosis in Elgadaref State, Eastern Sudan. Int J Hematol Dis. 4(1):4–8.
- Abdelrahman SSM. 2020. Prevalence of Brucellosis in cattle, goat and camel (Camelus dromedarius) during 2013-2018, Bahri Locality, Khartoum, Sudan. SUST J Agric Vet Sci. 21(2):37–49.
- Abdurahman OAS. 2004. Milk and meat from the camel: handbook on products and processing: vdf Hochschulverlag AG
- Abedi A-S, Hashempour-Baltork F, Alizadeh AM, Beikzadeh S, Hosseini H, Bashiry M, Taslikh M, Javanmardi F, Sheidaee Z, Sarlak Z, et al. 2020. The prevalence of Brucella spp. in dairy products in the Middle East region: a systematic review and meta-analysis. Acta Trop. 202:105241. doi:10.1016/j.actatropica.2019.105241.
- Ahmed AE, editor. 2015. A short note on camels export from the Sudan: importers conditions and associated practices. Special issue in the occasion of The Regional Conference of Camel Management and Production under Open Range System (RCCMPR); 2015; Khartoum-Sudan: Sudan University of Science and Technology.
- Ahmed SAM. 2020. Assessment of serological tests used for diagnosis of Brucellosis in camels and goats intended for exportation in Sudan. Khartoum, Sudan: Sudan University of Science and Technology.
- Ahmed SM. 2020. Impacts of drought, food security policy and climate change on performance of irrigation schemes in Sub-saharan Africa: the case of Sudan. Agric Water Manage. 232:106064. doi:10.1016/j.agwat.2020.106064.
- Ahmed HE, Ho A, Yagoub I, Sowar A, Noori Y, Atwa A, et al. 2018. Brucellosis screening in camels destined for export from two quarantine stations in Kordofan State. Sudan. Sudan J Vet Res. 2018(33):55–57.
- Ahmed MM, Ibrahaem HH, Shuaib YA, Elgadal AA, Shigidi MT. 2017. Sero-prevalence of anti-Brucella antibodies in camels in El-Gedarif state: a short communication. Scholars J Agric Vet Sci. 4(11):461–463.
- Akinyemi KO, Fakorede CO, Amisu KO, Wareth G. 2022. Human and animal brucellosis in Nigeria: a systemic review and meta-analysis in the last twenty-one years (2001–2021). Vet Sci. 9(8):384. doi:10.3390/vetsci9080384.
- Alhussain H, Zughaier SM, Gawish A, Mahmoud MH, Yassine HM, Al Thani A, Obied TEl, Al-Zeyara AM, Eltai NO. 2022. Seroprevalence of camel brucellosis in Qatar. Trop Anim Health Prod. 54(6):351. doi:10.1007/s11250-022-03335-z.
- Babikir IMO. 2022. Evaluation of different serological tests for diagnosis of brucellosis in camels and male goats intended export in Sudan. Khartoum, Sudan: Sudan University of Science and Technology.
- Bashir H, Abraheem HH, Khogly MI, Dafaallh EA, Idris SH, Bilal HAMA, Shuaib YA, Mohammed NE, Abdalla MA. 2022. Epidemiology of camel brucellosis intended for export from Kassala State – Eastern Sudan. Int J Appl Sci Biotechnol. 10(4):216–220. doi:10.3126/ijasbt.v10i4.48495.
- Blackwell P. 2010. East Africa’s Pastoralist Emergency: is climate change the straw that breaks the camel’s back? Third World Q. 31(8):1321–1338. doi:10.1080/01436597.2010.541085.
- Dadar M, Omar SS, Shahali Y, Fakhri Y, Godfroid J, Khaneghah AM. 2022. The prevalence of camel brucellosis and associated risk factors: a global meta-epidemiological study. Qual Assur Saf Crops Foods. 14(3):55–93. doi:10.15586/qas.v14i3.1088.
- Dafaalla E. 1962. Incidence of animal and human Brucellosis in the Sudan. Sudan J Vet Sci Anim Hus. 3:80–88.
- Damir HA, Kenyon SJ, Khalaf Alla AE, Idris OF. 1984. Brucella antibodies in Sudanese camels. Trop Anim Health Prod. 16(4):209–212. doi:10.1007/BF02265322.
- Dean AS, Crump L, Greter H, Hattendorf J, Schelling E, Zinsstag J. 2012. Clinical manifestations of human brucellosis: a systematic review and meta-analysis. PLoS Negl Trop Dis. 6(12):e1929. doi:10.1371/journal.pntd.0001929.
- El Ayis AA. 2022. Brucellosis and internal and blood protozoan parasites of camels in North Kordufan state, Sudan. Asian J Res Anim Vet Sci. 9(2):32–39.
- El Dirani OH. 2009. Constraints in the market chains for export of Sudanese sheep and sheep meat to the Middle East: ILRI (aka ILCA and ILRAD).
- El-Ansary E, Mohammed BA, Hamad A, Karom A. 2001. Brucellosis among animals and human contacts in eastern Sudan. Saudi Med J. 22(7):577–579.
- El-Diasty M, Salah K, El-Hofy F, Abd El Tawab A, Soliman E. 2022. Investigation of an outbreak of brucellosis in a mixed dairy farm and evaluation of a test and slaughter strategy to release the herd out of the quarantine. Ger J Vet Res. 2(1):1–9. doi:10.51585/gjvr.2022.1.0028.
- Elyass T. 2005. A comparative study on the occurrence of Brucellosis between Sudan and the Sultanate of Oman. Khartoum, Sudan: University of Khartoum;
- Erwa HH. 1966. Isolation of Brucella abortus in the Sudan. J Trop Med Hyg. 69(9):201–202.
- Gwet KL. 2008. Computing inter-rater reliability and its variance in the presence of high agreement. Br J Math Stat Psychol. 61(Pt 1):29–48. doi:10.1348/000711006X126600.
- Hamed YHB. 2021. Prevalence and risk factor of brucellosis in camels in North Kordofan State, Western Sudan. Khartoum, Sudan: Sudan University of Science and Technology.
- Hassan RO. 2013. Epidemiological aspects of human and animal brucellosis in Sudan. Khatroum, Sudan: University of Khartoum;
- Higgins JP, Thompson SG, Deeks JJ, Altman DG. 2003. Measuring inconsistency in meta-analyses. BMJ. 327(7414):557–560. doi:10.1136/bmj.327.7414.557.
- Hughes EC, Anderson NE. 2020. Zoonotic pathogens of dromedary camels in Kenya: a systematised review. Vet Sci. 7(3):103. doi:10.3390/vetsci7030103.
- Jordan Z, Lockwood C, Munn Z, Aromataris E. 2019. The updated Joanna Briggs Institute Model of Evidence-Based Healthcare. Int J Evid Based Healthc. 17(1):58–71. doi:10.1097/XEB.0000000000000155.
- Khoshnood S, Pakzad R, Koupaei M, Shirani M, Araghi A, Irani GM, Moradi M, Pakzad I, Sadeghifard N, Heidary M. 2022. Prevalence, diagnosis, and manifestations of brucellosis: a systematic review and meta-analysis. Front Vet Sci. 9:976215. doi:10.3389/fvets.2022.976215.
- Mahammed N. 2016. Prevalence and risk factors of camel brucellosis in Elgadrif state of Sudan. Khartoum, Sudan: Sudan University of Science and Technology.
- Mahmoud AS, Atif EA. 2012. Serological survey of cattle brucellosis in Eldein, eastern Darfur, Sudan. Afr J Microbiol Res. 6(31):6086–6090.
- Megid J, Mathias LA, Robles CA. 2010. Clinical manifestations of brucellosis in domestic animals and humans. TOVSJ. 4(1):119–126. doi:10.2174/1874318801004010119.
- Mohamed A, Salih S. 2004. A note of livestock brucellosis in Blue Nile state, Sudan. Sudan J Vet Sci Anim Husb. 19:89–90.
- Mohamed E, Elfadi A, El Sanousi EM. 2015. Epidemiological study of brucellosis in camels (Camelus dromedarius) in Khartoum State, Sudan. Int J Vet Sci. 4(1):39–43.
- Mohamed H. 2004. Studies on animal brucellosis in Red Sea State Sudan. Khartoum, Sudan: University Of Khartoum.
- Mohammed HA, Abdelgadir AE. 2016. Cross-sectional study of camel (Camelus dromedaries) brucellosis in the Red Sea state, Sudan. J Appl Sci Res. 4(2):67–77.
- Mokhtar MO, Abdelaziz AA, Sarah M, Ahmed AM. 2007. Survey of brucellosis among sheep, goat, camel, and cattle in Kassala area eastern Sudan. J Anim Vet Adv. 6(5):635–637.
- Musa L, Riessmann M, Ishag I. 2013. Evaluation of serological tests for diagnosis of brucellosis in camels for export and control purposes in the Sudan. J Anim Prod Adv. 3(2):28–37. doi:10.5455/japa.20130205115834.
- Musa M, Shigidi M. 2001. Brucellosis in camels in intensive animal breeding areas of Sudan. Implications in abortion and early-life infection. Revue d’élevage Méd Vét Pays Tropicaux. 54(1):11–15.
- Musa M. 2004. A serological study on equine brucellosis in Darfur, Western Sudan. Sudan J Vet Res. 19(2):7–11.
- Omer M, Musa M, Bakhiet M, Perrett L. 2010. Brucellosis in camels, cattle and humans: associations and evaluation of serological tests used for diagnosis of the disease in certain nomadic localities in Sudan. Rev Sci Technol. 29(3):663–669. doi:10.20506/rst.29.3.2003.
- Page MJ, Moher D, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, et al. 2021. PRISMA 2020 explanation and elaboration: updated guidance and exemplars for reporting systematic reviews. BMJ. 372:n160. doi:10.1136/bmj.n160.
- Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV. 2006. The new global map of human brucellosis. Lancet Infect Dis. 6(2):91–99. doi:10.1016/S1473-3099(06)70382-6.
- Raga IO. 2000. Studies on brucellosis in camel and cattle in Darfur States. Khartoum, Sudan: University of Khartoum;
- Robinson A. 2003. Guidelines for coordinated human and animal brucellosis surveillance. Rome, Italy: FAO; p. 45.
- Roth F, Zinsstag J, Orkhon D, Chimed-Ochir G, Hutton G, Cosivi O. 2003. Human health benefits from livestock vaccination for brucellosis: case study. Bull World Health Organ. 81(12):867–876.
- Seleem MN, Boyle SM, Sriranganathan N. 2010. Brucellosis: a re-emerging zoonosis. Vet Microbiol. 140(3-4):392–398. doi:10.1016/j.vetmic.2009.06.021.
- Sprague LD, Al-Dahouk S, Neubauer H. 2012. A review on camel brucellosis: a zoonosis sustained by ignorance and indifference. Pathog Glob Health. 106(3):144–149. doi:10.1179/2047773212Y.0000000020.
- Suresh KP, Patil SS, Nayak A, Dhanze H, Rajamani S, Shivamallu C, Cull CA, Amachawadi RG. 2022. Prevalence of brucellosis in livestock of African and Asian continents: a systematic review and meta-analysis. Front Vet Sci. 9:923657. doi:10.3389/fvets.2022.923657.
- Tadesse G. 2016. Brucellosis seropositivity in animals and humans in Ethiopia: a meta-analysis. PLoS Negl Trop Dis. 10(10):e0005006. doi:10.1371/journal.pntd.0005006.
- Williams H. 1939. Annual report of the Sudan Veterinary Service. 1940.
- Yagoub IA, Mohamed AA, Salim MO. 1990. Serological survey of Brucella abortus antibody prevalence in the one-humped camel (Camelus dromedarius) from eastern Sudan. Rev Elev Med Vet Pays Trop. 43(2):167–171. doi:10.19182/remvt.8838.
- Yahya BAI. 2015. Sero-epidemiological study of camel brucellosis Camelus dromedarius and associated risk factors in the Butana Plain Area and Al-Gadarief State–Sudan. Khartoum, Sudan: Sudan University of Science and Technology;
- Younan M, Bornstein S, Gluecks I. 2016. MERS and the dromedary camel trade between Africa and the Middle East. Trop Anim Health Prod. 48(6):1277–1282. doi:10.1007/s11250-016-1089-3.
- Zein AM. 2015. Short communication: prevalence of brucellosis in farm animals in Northern State, Sudan. Sudan J Vet Res. 30:43–44.