Serological and bacterial prevalence of Brucella spp. in suspected patients: a risk factor analysis in North Khorasan, Iran
-
Niloofar Sadooghi
,
Saeed Alamian
,
Hamed Ghasemzadeh Moghadam
,
Mohammad Yazdanmanesh
,
Maryam Dadar
Abstract
Background and Objectives: Brucellosis, a zoonotic bacterial disease caused by Brucella, affects humans and domestic animals, leading to significant economic loss. This study examined suspected cases in North Khorasan, Iran, to understand the prevalence of infection and its characteristics in this region.
Materials and Methods: Blood specimens were collected from 200 patients suspected of brucellosis after obtaining informed consent. Serum samples were tested using RBPT, Wright, and 2-ME agglutination tests. Blood samples were cultured on Brucella agar, and positive cultures underwent biotyping and PCR assays. A questionnaire identified correlated risk factors.
Results: RBPT, Wright, and 2-ME tests showed 25% brucellosis seroprevalence in symptomatic patients. In contrast, the prevalence was 2.5% among those with positive blood cultures. Notably, all culture-positive patients were also serologically positive, with titers exceeding 1:320 in Wright and 2-ME tests. Most positive cases were in people in their 30s, with B. melitensis biovar 1 identified as the causative agent, and the results were confirmed by multiplex PCR. Significant risk factors include contact with livestock and consumption of raw milk (P < 0.0001).
Conclusion: The findings highlighted the importance of comprehensive diagnostic approaches for accurate identification of brucellosis. Furthermore, education regarding close contact with animals and pasteurization of dairy products is essential for controlling human brucellosis.
1. Chen JD, Ke CW, Deng X, Jiang S, Liang W, Ke BX, et al. Brucellosis in guangdong province, people's republic of China, 2005-2010. Emerg Infect Dis 2013; 19: 817-818.
2. Percin D. Microbiology of Brucella. Recent Pat Antiinfect Drug Discov 2013; 8: 13-17.
3. Whatmore AM. Current understanding of the genetic diversity of Brucella, an expanding genus of zoonotic pathogens. Infect Genet Evol 2009; 9: 1168-1184.
4. Laine CG, Johnson VE, Scott HM, Arenas-Gamboa AM. Global estimate of human brucellosis incidence. Emerg Infect Dis 2023; 29: 1789-1797.
5. Dadar M, Shahali Y, Whatmore AM. Human brucellosis caused by raw dairy products: A review on the occurrence, major risk factors and prevention. Int J Food Microbiol 2019; 292: 39-47.
6. Dadar M, Shahali Y, Alamian S. Isolation of Brucella melitensis biovar 1 from human milk confirms breastfeeding as a possible route for infant infection. Microb Pathog 2021; 157: 104958.
7. Ay N, Kaya S, Anil M, Alp V, Beyazit U, Yuksel E, et al. Pulmonary involvement in brucellosis, a rare complication of renal transplant: case report and brief review. Exp Clin Transplant 2018; 16: 757-760.
8. Doganay M, Aygen B. Human brucellosis: an overview. Int J Infect Dis 2003; 7: 173-182.
9. Franco MP, Mulder M, Gilman RH, Smits HL. Human brucellosis. Lancet Infect Dis 2007; 7: 775-786.
10. Dean AS, Crump L, Greter H, Schelling E, Zinsstag J. Global burden of human brucellosis: A systematic review of disease frequency. PLoS Negl Trop Dis 2012; 6(10): e1865.
11. Dadar M, Alamian S, Behrozikhah AM, Yazdani F, Kalantari A, Etemadi A, et al. Molecular identification of Brucella species and biovars associated with animal and human infection in Iran. Vet Res Forum 2019; 10: 315-321.
12. Dadar M, Tabibi R, Alamian S, Caraballo-Arias Y, Mrema EJ, Mlimbila J, et al. Safety concerns and potential hazards of occupational brucellosis in developing countries: A review. J Public Health 2023; 31: 1681-1690.
13. Akkina J, Burkom H, Estberg L, Carpenter L, Hennessey M, Meidenbauer K. Feral swine commercial slaughter and condemnation at federally inspected slaughter establishments in the United States 2017–2019. Front Vet Sci 2021; 8: 690346.
14. Schelling E, Diguimbaye C, Daoud S, Nicolet J, Boerlin P, Tanner M, et al. Brucellosis and Q-fever seroprevalences of nomadic pastoralists and their livestock in Chad. Prev Vet Med 2003; 61: 279-293.
15. Al-Mashhadany D. Prevalence of brucellosis in human and camels in Thamar Province/Yemen. J Saudi Soc Agric Sci 2014; 13: 108-132.
16. Chalabiani S, Khodadad Nazari M, Razavi Davoodi N, Shabani M, Mardani M, Sarafnejad A, et al. The prevalence of Brucellosis in different provinces of Iran during 2013–2015. Iran J Public Health 2019; 48: 132-138.
17. Etemadi A, Moniri R, Saffari M, Akbari H, Alamian S, Behrozikhah AM. Epidemiological, molecular characterization and risk factors of human brucellosis in Iran. Asian Pac J Trop Med 2020; 13: 169-175.
18. Khalid HM. Seroprevalence and associated risk factors of brucellosis among human population in duhok city, Iraq. Infect Drug Resist 2023; 16: 2805-2811.
19. Nielsen K. Diagnosis of brucellosis by serology. Vet Microbiol 2002; 90: 447-459.
20. Ewalt DR, Bricker BJ. Validation of the abbreviated Brucella AMOS PCR as a rapid screening method for differentiation of Brucella abortus field strain isolates and the vaccine strains, 19 and RB51. J Clin Microbiol 2000; 38: 3085-3086.
21. Lopez-Goñi I, Garcia-Yoldi D, Marín C, De Miguel M, Munoz PM, Blasco JM, et al. Evaluation of a multiplex PCR assay (Bruce-ladder) for molecular typing of all Brucella species, including the vaccine strains. J Clin Microbiol 2008; 46: 3484-3487.
22. Yagupsky P, Morata P, Colmenero JD. Laboratory diagnosis of human brucellosis. Clin Microbiol Rev 2019; 33(1): e00073-19.
23. Ebrahimpour S, Youssefi MR, Karimi N, Kaighobadi M, Tabaripour R. The prevalence of human Brucellosis in Mazandaran province, Iran. Afr J Microbiol Res 2012; 6: 4090-4094.
24. Nikokar I, Hosseinpour M, Asmar M, Pirmohbatei S, Hakeimei F, Razavei MT. Seroprevalence of Brucellosis among high risk individuals in Guilan, Iran. J Res Med Sci 2011; 16: 1366-1371.
25. Niaz S, Raqeeb A, Khan A, Nasreen, Amir S, Zhu L, et al. Status of human brucellosis in district Malakand, Khyber Pakhtunkhwa, Pakistan. J Infect Public Health 2021; 14: 423-427.
26. Gafirita J, Kiiza G, Murekatete A, Ndahayo LL, Tuyisenge J, Mashengesho V, et al. Seroprevalence of brucellosis among patients attending a district hospital in Rwanda. Am J Trop Med Hyg 2017; 97: 831-835.
27. Aypak C, Altunsoy A, Çelik AK. Epidemiological and clinical aspects of human brucellosis in eastern Anatolia. J Nippon Med Sch 2012; 79: 343-348.
28. Bansal Y, Aggarwal A, Gadepalli R, Nag VL. Seroprevalence of brucellosis in Western Rajasthan: A study from a tertiary care centre. Indian J Med Microbiol 2019; 37: 426-432.
29. Dadar M, Godfroid J. Main risk factors associated with small and large ruminant brucellosis. Indian J Anim Sci 2021; 91: 885-890.
30. Dadar M, Omar SS, Shahali Y, Fakhri Y, Godfroid J, Khaneghah AM. The prevalence of camel brucellosis and associated risk factors: a global meta-epidemiological study. Qual Assur Saf Crops Foods 2022; 14: 55-93.
31. Dadar M, Tiwari R, Sharun K, Dhama K. Importance of brucellosis control programs of livestock on the improvement of one health. Vet Q 2021; 41: 137-151.
32. Kiambi SG, Fèvre EM, Omolo J, Oundo J, De Glanville WA. Risk factors for acute human brucellosis in Ijara, north-eastern Kenya. PLoS Negl Trop Dis 2020; 14(4): e0008108.
33. Musallam I, Ndour AP, Yempabou D, Ngong CC, Dzousse MF, Mouiche-Mouliom MM, et al. Brucellosis in dairy herds: A public health concern in the milk supply chains of West and Central Africa. Acta Trop 2019; 197: 105042.
34. Jennings GJ, Hajjeh RA, Girgis FY, Fadeel MA, Maksoud MA, Wasfy MO, et al. Brucellosis as a cause of acute febrile illness in Egypt. Trans R Soc Trop Med Hyg 2007; 101: 707-713.
35. Adabi M, Karami M, Keramat F, Alikhani MY, Bakhtiari S. Serological and molecular investigation of human brucellosis in participants of Famenin brucellosis cohort study, Hamadan, Iran. Iran J Microbiol 2021; 13: 319-324.
36. Keramat F, Karami M, Alikhani MY, Bashirian S, Moghimbeigi A, Adabi M. Cohort profile: Famenin brucellosis cohort study. J Res Health Sci 2019; 19(3): e00453.
37. Al-Sekait MA. Epidemiology of brucellosis in Al medina region, Saudi Arabia. J Family Community Med 2000; 7: 47-53.
38. Niaz S, Raqeeb A, Khan A, Nasreen, Amir S, Zhu L, et al. Status of human brucellosis in district Malakand, Khyber Pakhtunkhwa, Pakistan. J Infect Public Health 2021; 14: 423-427.
39. Rahman AK, Dirk B, Fretin D, Saegerman C, Ahmed MU, Muhammad N, et al. Seroprevalence and risk factors for brucellosis in a high-risk group of individuals in Bangladesh. Foodborne Pathog Dis 2012; 9: 190-197.
40. Tumwine G, Matovu E, Kabasa JD, Owiny DO, Majalija S. Human brucellosis: seroprevalence and associated risk factors in agro-pastoral communities of Kiboga District, Central Uganda. BMC Public Health 2015; 15: 900.
41. Alzuheir I, Al Zabadi H, Abu Helal M. Occupational exposure assessment and seroprevalence of Brucella specific antibodies among veterinarians in the northern palestine. Front Vet Sci 2022; 8: 813900.
42. Gür A, Geyik MF, Dikici B, Nas K, Çevik R, Saraç J, et al. Complications of brucellosis in different age groups: a study of 283 cases in southeastern Anatolia of Turkey. Yonsei Med J 2003; 44: 33-44.
43. Kairu-Wanyoike S, Nyamwaya D, Wainaina M, Lindahl J, Ontiri E, Bukachi S, et al. Positive association between Brucella spp. seroprevalences in livestock and humans from a cross-sectional study in Garissa and Tana River Counties, Kenya. PLoS Negl Trop Dis 2019; 13(10): e0007506.
44. Mangalgi SS, Sajjan AG, Mohite ST, Kakade SV. Serological, clinical, and epidemiological profile of human brucellosis in rural India. Indian J Community Med 2015; 40: 163-167.
45. Dadar M, Alamian S, Tadayon K, Ashford RT, Whatmore AM. Molecular characterization of zoonotic Brucella species isolated from animal and human samples in Iran. Acta Trop 2022; 229: 106363.
46. Malik S, Sarwar I, Rauf A, Haroon MZ. Seroprevalence of brucellosis among patients presenting with non–specific symptoms at Ayub teaching hospital Abbottabad. J Ayub Med Coll Abbottabad 2018; 30: 566-570.
47. Elfaki MG, Uz-Zaman T, Al-Hokail AA, Nakeeb SM. Detection of brucella DNA in sera from patients with brucellosis by polymerase chain reaction. Diagn Microbiol Infect Dis 2005; 53: 1-7.
48. Dal T, Kara SS, Cikman A, Balkan CE, Acıkgoz ZC, Zeybek H, et al. Comparison of multiplex real-time polymerase chain reaction with serological tests and culture for diagnosing human brucellosis. J Infect Public Health 2019; 12: 337-342.
49. Dadar M, Al-Khaza'leh J, Fakhri Y, Akar K, Ali S, Shahali Y. Human brucellosis and associated risk factors in the Middle East region: A comprehensive systematic review, meta-analysis, and meta-regression. Heliyon 2024; 10(14): e34324.
2. Percin D. Microbiology of Brucella. Recent Pat Antiinfect Drug Discov 2013; 8: 13-17.
3. Whatmore AM. Current understanding of the genetic diversity of Brucella, an expanding genus of zoonotic pathogens. Infect Genet Evol 2009; 9: 1168-1184.
4. Laine CG, Johnson VE, Scott HM, Arenas-Gamboa AM. Global estimate of human brucellosis incidence. Emerg Infect Dis 2023; 29: 1789-1797.
5. Dadar M, Shahali Y, Whatmore AM. Human brucellosis caused by raw dairy products: A review on the occurrence, major risk factors and prevention. Int J Food Microbiol 2019; 292: 39-47.
6. Dadar M, Shahali Y, Alamian S. Isolation of Brucella melitensis biovar 1 from human milk confirms breastfeeding as a possible route for infant infection. Microb Pathog 2021; 157: 104958.
7. Ay N, Kaya S, Anil M, Alp V, Beyazit U, Yuksel E, et al. Pulmonary involvement in brucellosis, a rare complication of renal transplant: case report and brief review. Exp Clin Transplant 2018; 16: 757-760.
8. Doganay M, Aygen B. Human brucellosis: an overview. Int J Infect Dis 2003; 7: 173-182.
9. Franco MP, Mulder M, Gilman RH, Smits HL. Human brucellosis. Lancet Infect Dis 2007; 7: 775-786.
10. Dean AS, Crump L, Greter H, Schelling E, Zinsstag J. Global burden of human brucellosis: A systematic review of disease frequency. PLoS Negl Trop Dis 2012; 6(10): e1865.
11. Dadar M, Alamian S, Behrozikhah AM, Yazdani F, Kalantari A, Etemadi A, et al. Molecular identification of Brucella species and biovars associated with animal and human infection in Iran. Vet Res Forum 2019; 10: 315-321.
12. Dadar M, Tabibi R, Alamian S, Caraballo-Arias Y, Mrema EJ, Mlimbila J, et al. Safety concerns and potential hazards of occupational brucellosis in developing countries: A review. J Public Health 2023; 31: 1681-1690.
13. Akkina J, Burkom H, Estberg L, Carpenter L, Hennessey M, Meidenbauer K. Feral swine commercial slaughter and condemnation at federally inspected slaughter establishments in the United States 2017–2019. Front Vet Sci 2021; 8: 690346.
14. Schelling E, Diguimbaye C, Daoud S, Nicolet J, Boerlin P, Tanner M, et al. Brucellosis and Q-fever seroprevalences of nomadic pastoralists and their livestock in Chad. Prev Vet Med 2003; 61: 279-293.
15. Al-Mashhadany D. Prevalence of brucellosis in human and camels in Thamar Province/Yemen. J Saudi Soc Agric Sci 2014; 13: 108-132.
16. Chalabiani S, Khodadad Nazari M, Razavi Davoodi N, Shabani M, Mardani M, Sarafnejad A, et al. The prevalence of Brucellosis in different provinces of Iran during 2013–2015. Iran J Public Health 2019; 48: 132-138.
17. Etemadi A, Moniri R, Saffari M, Akbari H, Alamian S, Behrozikhah AM. Epidemiological, molecular characterization and risk factors of human brucellosis in Iran. Asian Pac J Trop Med 2020; 13: 169-175.
18. Khalid HM. Seroprevalence and associated risk factors of brucellosis among human population in duhok city, Iraq. Infect Drug Resist 2023; 16: 2805-2811.
19. Nielsen K. Diagnosis of brucellosis by serology. Vet Microbiol 2002; 90: 447-459.
20. Ewalt DR, Bricker BJ. Validation of the abbreviated Brucella AMOS PCR as a rapid screening method for differentiation of Brucella abortus field strain isolates and the vaccine strains, 19 and RB51. J Clin Microbiol 2000; 38: 3085-3086.
21. Lopez-Goñi I, Garcia-Yoldi D, Marín C, De Miguel M, Munoz PM, Blasco JM, et al. Evaluation of a multiplex PCR assay (Bruce-ladder) for molecular typing of all Brucella species, including the vaccine strains. J Clin Microbiol 2008; 46: 3484-3487.
22. Yagupsky P, Morata P, Colmenero JD. Laboratory diagnosis of human brucellosis. Clin Microbiol Rev 2019; 33(1): e00073-19.
23. Ebrahimpour S, Youssefi MR, Karimi N, Kaighobadi M, Tabaripour R. The prevalence of human Brucellosis in Mazandaran province, Iran. Afr J Microbiol Res 2012; 6: 4090-4094.
24. Nikokar I, Hosseinpour M, Asmar M, Pirmohbatei S, Hakeimei F, Razavei MT. Seroprevalence of Brucellosis among high risk individuals in Guilan, Iran. J Res Med Sci 2011; 16: 1366-1371.
25. Niaz S, Raqeeb A, Khan A, Nasreen, Amir S, Zhu L, et al. Status of human brucellosis in district Malakand, Khyber Pakhtunkhwa, Pakistan. J Infect Public Health 2021; 14: 423-427.
26. Gafirita J, Kiiza G, Murekatete A, Ndahayo LL, Tuyisenge J, Mashengesho V, et al. Seroprevalence of brucellosis among patients attending a district hospital in Rwanda. Am J Trop Med Hyg 2017; 97: 831-835.
27. Aypak C, Altunsoy A, Çelik AK. Epidemiological and clinical aspects of human brucellosis in eastern Anatolia. J Nippon Med Sch 2012; 79: 343-348.
28. Bansal Y, Aggarwal A, Gadepalli R, Nag VL. Seroprevalence of brucellosis in Western Rajasthan: A study from a tertiary care centre. Indian J Med Microbiol 2019; 37: 426-432.
29. Dadar M, Godfroid J. Main risk factors associated with small and large ruminant brucellosis. Indian J Anim Sci 2021; 91: 885-890.
30. Dadar M, Omar SS, Shahali Y, Fakhri Y, Godfroid J, Khaneghah AM. The prevalence of camel brucellosis and associated risk factors: a global meta-epidemiological study. Qual Assur Saf Crops Foods 2022; 14: 55-93.
31. Dadar M, Tiwari R, Sharun K, Dhama K. Importance of brucellosis control programs of livestock on the improvement of one health. Vet Q 2021; 41: 137-151.
32. Kiambi SG, Fèvre EM, Omolo J, Oundo J, De Glanville WA. Risk factors for acute human brucellosis in Ijara, north-eastern Kenya. PLoS Negl Trop Dis 2020; 14(4): e0008108.
33. Musallam I, Ndour AP, Yempabou D, Ngong CC, Dzousse MF, Mouiche-Mouliom MM, et al. Brucellosis in dairy herds: A public health concern in the milk supply chains of West and Central Africa. Acta Trop 2019; 197: 105042.
34. Jennings GJ, Hajjeh RA, Girgis FY, Fadeel MA, Maksoud MA, Wasfy MO, et al. Brucellosis as a cause of acute febrile illness in Egypt. Trans R Soc Trop Med Hyg 2007; 101: 707-713.
35. Adabi M, Karami M, Keramat F, Alikhani MY, Bakhtiari S. Serological and molecular investigation of human brucellosis in participants of Famenin brucellosis cohort study, Hamadan, Iran. Iran J Microbiol 2021; 13: 319-324.
36. Keramat F, Karami M, Alikhani MY, Bashirian S, Moghimbeigi A, Adabi M. Cohort profile: Famenin brucellosis cohort study. J Res Health Sci 2019; 19(3): e00453.
37. Al-Sekait MA. Epidemiology of brucellosis in Al medina region, Saudi Arabia. J Family Community Med 2000; 7: 47-53.
38. Niaz S, Raqeeb A, Khan A, Nasreen, Amir S, Zhu L, et al. Status of human brucellosis in district Malakand, Khyber Pakhtunkhwa, Pakistan. J Infect Public Health 2021; 14: 423-427.
39. Rahman AK, Dirk B, Fretin D, Saegerman C, Ahmed MU, Muhammad N, et al. Seroprevalence and risk factors for brucellosis in a high-risk group of individuals in Bangladesh. Foodborne Pathog Dis 2012; 9: 190-197.
40. Tumwine G, Matovu E, Kabasa JD, Owiny DO, Majalija S. Human brucellosis: seroprevalence and associated risk factors in agro-pastoral communities of Kiboga District, Central Uganda. BMC Public Health 2015; 15: 900.
41. Alzuheir I, Al Zabadi H, Abu Helal M. Occupational exposure assessment and seroprevalence of Brucella specific antibodies among veterinarians in the northern palestine. Front Vet Sci 2022; 8: 813900.
42. Gür A, Geyik MF, Dikici B, Nas K, Çevik R, Saraç J, et al. Complications of brucellosis in different age groups: a study of 283 cases in southeastern Anatolia of Turkey. Yonsei Med J 2003; 44: 33-44.
43. Kairu-Wanyoike S, Nyamwaya D, Wainaina M, Lindahl J, Ontiri E, Bukachi S, et al. Positive association between Brucella spp. seroprevalences in livestock and humans from a cross-sectional study in Garissa and Tana River Counties, Kenya. PLoS Negl Trop Dis 2019; 13(10): e0007506.
44. Mangalgi SS, Sajjan AG, Mohite ST, Kakade SV. Serological, clinical, and epidemiological profile of human brucellosis in rural India. Indian J Community Med 2015; 40: 163-167.
45. Dadar M, Alamian S, Tadayon K, Ashford RT, Whatmore AM. Molecular characterization of zoonotic Brucella species isolated from animal and human samples in Iran. Acta Trop 2022; 229: 106363.
46. Malik S, Sarwar I, Rauf A, Haroon MZ. Seroprevalence of brucellosis among patients presenting with non–specific symptoms at Ayub teaching hospital Abbottabad. J Ayub Med Coll Abbottabad 2018; 30: 566-570.
47. Elfaki MG, Uz-Zaman T, Al-Hokail AA, Nakeeb SM. Detection of brucella DNA in sera from patients with brucellosis by polymerase chain reaction. Diagn Microbiol Infect Dis 2005; 53: 1-7.
48. Dal T, Kara SS, Cikman A, Balkan CE, Acıkgoz ZC, Zeybek H, et al. Comparison of multiplex real-time polymerase chain reaction with serological tests and culture for diagnosing human brucellosis. J Infect Public Health 2019; 12: 337-342.
49. Dadar M, Al-Khaza'leh J, Fakhri Y, Akar K, Ali S, Shahali Y. Human brucellosis and associated risk factors in the Middle East region: A comprehensive systematic review, meta-analysis, and meta-regression. Heliyon 2024; 10(14): e34324.
| Files | ||
| Issue | Vol 16 No 5 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i5.16797 | |
| Keywords | ||
| Brucellosis; Humans; Multiplex polymerase chain reaction; Blood culture; Risk factors | ||
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How to Cite
1.
Sadooghi N, Alamian S, Ghasemzadeh Moghadam H, Yazdanmanesh M, Dadar M. Serological and bacterial prevalence of Brucella spp. in suspected patients: a risk factor analysis in North Khorasan, Iran. Iran J Microbiol. 2024;16(5):639-647.
