Epidemiological Trends and Animal–Human Relationships of Brucellosis in Constantine Province, Eastern Algeria from 2015 to 2023

Abstract

Objective: The objectives of this study were to characterise the epidemiology of human and animal brucellosis in the eastern Algerian province of Constantine, and to identify the interactions between humans and animals, to establish strategies from a unique health perspective considering the context of endemicity and eradication challenges.

Methods: Data collected from official institutions regarding brucellosis in humans and animals in Constantine and seven other provinces from 2015 to 2023 (until August 2022 for animals) were analysed to estimate temporal trends, alert thresholds, and correlations between humans and animals.

Results: A total of 163 brucellosis cases in humans were recorded in Constantine between 2015 and 2023, and the annual average was 1.47/100,000. The epidemic threshold was exceeded in 2021 and 2022. Males and residents 20–44 years of age were the most affected groups. In cattle, the prevalence was 1.32%, and the screening rate was below 7.5%. The only significant correlation was observed between humans and goats (r = −0.747, p = 0.03). The southern Constantine region was the most affected.

Conclusion: Brucellosis is an underestimated public health threat in Algeria. Gaps in its management include inadequate screening of goats, insufficient vaccination coverage and underreporting. The implementation of more comprehensive surveillance programmes is imperative.

Keywords

human brucellosis / incidence / animal brucellosis / zoonosis / epidemic threshold / One Health / Algeria

References

[1] Qureshi KA, Parvez A, Fahmy NA, Abdel Hady BH, Kumar S, Ganguly A, et al. Brucellosis: epidemiology, pathogenesis, diagnosis and treatment-a comprehensive review. Ann Med. 2023; 55(2): 2295398.

[2] Laine CG, Johnson VE, Scott HM, Arenas-Gamboa AM. Global estimate of human brucellosis incidence. Emerg Infect Dis. 2023; 29(9): 1789-1797.

[3] Gibbs SJ. Infectious diseases: brucellosis. In Encyclopedia of Dairy Sciences. 3rd edition. Edited by McSweeney PLH, McNamara JP. Oxford: Academic Press; 2022: 317-322.

[4] Young EJ. An overview of human brucellosis. Clin Infect Dis. 1995; 21(2): 283-290.

[5] Zhou K, Wu B, Pan H, Paudyal N, Jiang J, Zhang L, et al. One health approach to address zoonotic brucellosis: a spatiotemporal associations study between animals and humans. Front Vet Sci. 2020; 7: 521.

[6] de Figueiredo P, Ficht TA, Rice-Ficht A, Rossetti CA, Adams LG. Pathogenesis and immunobiology of brucellosis: review of Brucella-host interactions. Am J Pathol. 2015; 185(6): 1505-1517.

[7] Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV. The new global map of human brucellosis. Lancet Infect Dis. 2006; 6(2): 91-99.

[8] Ducrotoy MJ, Bardosh KL. How do you get the Rose Bengal Test at the point-of-care to diagnose brucellosis in Africa? The importance of a systems approach. Acta Trop. 2017; 165: 33-39.

[9] Lounes N, Cherfa MA, Le Carrou G, Bouyoucef A, Jay M, Garin-Bastuji B, et al. Human brucellosis in Maghreb: existence of a lineage related to socio-historical connections with Europe. PLoS One. 2014; 9(12): e115319.

[10] Liu Z, Gao L, Wang M, Yuan M, Li Z. Long ignored but making a comeback: a worldwide epidemiological evolution of human brucellosis. Emerg Microbes Infect. 2024; 13(1): 2290839.

[11] Benhabyles N, Benkirane A, Boudilmi B, Benchouk S, Bouayoun H. Epidémiologie de la brucellose humaine et animale au Maghreb. In Prevention of Brucellosis in the Mediterranean Countries: Proceedings of the International Seminar . 28-30 October 1991; Malta. Edited by CIHEAM, CEC, MINAG, Valletta, Malta. CIHEAM Publication n°1. Pudoc Scientific Publishers Wageningen; 1992.

[12] Lounes N, Yahiaoui D, Taftaf D, Zenia S. A survey on the occupational exposure of veterinarians to brucellosis in Algeria. German J Microbiol. 2022; 2(2): 28-35.

[13] Djellata N, Yahimi A, Hanzen C, Saegerman C. Survey of the prevalence of bovine abortions and notification and management practices by veterinary practitioners in Algeria. Rev Sci Tech. 2020; 39(3): 947-968.

[14] Moriyón I, Blasco JM, Letesson JJ, De Massis F, Moreno E. Brucellosis and one health: inherited and future challenges. Microorganisms. 2023; 11(8): 2070.

[15] Aggad H. Serological studies of animal brucellosis Algeria. Assiut Vet Med J. 2003; 49(98): 121-130.

[16] Bachir P, Kechih S, Berber A, Yamani RRT. An inquiry about ruminants epidemiologic brucellosis in some Algerian departments. Bull Univ Agric Sci Vet Med Cluj Napoca. 2009; 66.

[17] Gabli A, Agabou A, Gabli Z. Brucellosis in nomadic pastoralists and their goats in two provinces of the eastern Algerian high plateaus. Trop Anim Health Prod. 2015; 47(6): 1043-1048.

[18] Kardjadj M, Kouidri B, Metref D, Luka PD, Ben-Mahdi MH. Abortion and various associated risk factors in small ruminants in Algeria. Prev Vet Med. 2016; 123: 97-101.

[19] Ramdani N, Boussena S, Bouaziz O, Moula N. Brucellosis in small ruminant: seroprevalence, risk factors, and distribution in the southeast of Algeria. Trop Anim Health Prod. 2022; 54(4): 245.

[20] Derdour SY, Hafsi F, Azzag N, Tennah S, Laamari A, China B, et al. Prevalence of the main infectious causes of abortion in dairy cattle in Algeria. J Vet Res. 2017; 61: 337-343.

[21] Khames M, Mick V, de Miguel MJ, Girault G, Conde-Álvarez R, Khelef D, et al. The characterization of Brucella strains isolated from cattle in Algeria reveals the existence of a B. abortus lineage distinct from European and Sub-Saharan Africa strains. Vet Microbiol. 2017; 211: 124-128.

[22] Lounes N, Melzer F, Sayour AE, Maamar HT, Rahal K, Benamrouche N, et al. Identification, geographic distribution and risk factors of Brucella abortus and Brucella melitensis infection in cattle in Algeria . Vet Microbiol. 2021; 254: 109004.

[23] Akermi SE, L’Hadj M, Selmane S. Epidemiology and time series analysis of human brucellosis in Tebessa province, Algeria, from 2000 to 2020. J Res Health Sci. 2022; 22(1): e00544.

[24] Yahiaoui WI, Dahmani A. Brucellosis in hospitalized patients and their animals in the agro-pastoral region of Theniet El Had (Algeria) during ten years (2013−2023). IDCases. 2024; 36: e01945.

[25] Aggad H, Boukraa L. Prevalence of bovine and human brucellosis in western Algeria: comparison of screening tests. East Mediterr Health J. 2006; 12(1-2): 119-128.

[26] Kardjadj M. The epidemiology of human and animal brucellosis in Algeria. J Bacteriol Mycol. 2016; 3(2): 1025.

[27] INSP (Institut National de Santé Publique). Bulletin Epidémiologique Régional BER-Est. 2023. Available from: https://www.insp.dz/images/PDF/ORS%20Constantine/Bulletin_Epidemiologique_Regional_BER_Est.pdf Accessed on date June 29, 2024.

[28] ANIREF (Agence Nationale d’Intermédiation et de Régulation Foncière). Agence Nationale d’Intermédiation et de Régulation Foncière. Monographie wilaya de Constantine; 2021. Available from: https://interieur.gov.dz/Monographie/index.php?wil=25.

[29] DSA Constantine. Directorate of Agricultural services of Constantine province, Algerian Ministry of Agriculture and Rural development. 2022.

[30] IBM Corp. Released 2015. IBM SPSS Statistics for Windows, Version 23.0. Armonk, NY: IBM Corp.

[31] Farrington CP, Andrews NJ, Beale AD, Catchpole MA. A statistical algorithm for the early detection of outbreaks of infectious disease. J R Stat Soc Ser A. 1996; 159(3): 547-563.

[32] QGIS.org. QGIS Geographic Information System. QGIS Association; 2024. Available from: http://www.qgis.org.

[33] Khamassi Khbou M, Htira S, Harabech K, Benzarti M. First case-control study of zoonotic brucellosis in Gafsa district, Southwest Tunisia. One Health. 2017; 5: 21-26.

[34] Ducrotoy MJ, Ammary K, Ait Lbacha H, Zouagui Z, Mick V, Prevost L, et al. Narrative overview of animal and human brucellosis in Morocco: intensification of livestock production as a driver for emergence? Infect Dis Poverty. 2015; 4(1): 57.

[35] Nawana T, Ezzine H, Cherkaoui I, Meski FZ, Youbi M. Brucellosis at the human-animal interface, Morocco, 2002-2019. Int J Infect Dis. 2022; 116: S75.

[36] Akar K, Öz GY. The first report of Brucella melitensis biovar 2 strain isolated from cattle in Turkey . Ger J Vet Res. 2023; 3(2): 11-15.

[37] MADR (Ministère de l’agriculture et du Développement Rural). Statistiques agricoles SERIE-B-2019. 2022. Available from: https://madr.gov.dz/wp-content/uploads/2022/04/SERIE-B-2019.pdf.

[38] INSP (Institut National de Santé Publique). Relevé Epidémiologique Mensuel « R.E.M » Algérie. Volume XXXIII. 2022. Available from: https://www.insp.dz/images/PDF/Epidemio/REM_annuel_2022.pdf.

[39] INSP (Institut National de Santé Publique). Bulletin Epidémiologique de l’ORS d’ORAN. 2023. Available from: https://insp.dz/images/PDF/ORS20Oran/BulletinEpidemiologiqueTrimestrield’oran_N_22.

[40] Khezzani B, Narimane Aouachria A, Khechekhouche EA, Djaballah S, Djedidi T, Bosilkovski M. Caractéristiques épidémiologiques de la brucellose humaine dans la province d’El-Oued, sud-est algérien. Sante Publique. 2021; 33(2): 275-284.

[41] De Massis F, Di Girolamo A, Petrini A, Pizzigallo E, Giovannini A. Correlation between animal and human brucellosis in Italy during the period 1997-2002. Clin Microbiol Infect. 2005; 11(8): 632-636.

[42] Babo SAY, Fokou G, Yapi RB, Mathew C, Dayoro AK, Kazwala RR, et al. Gendered asymmetry of access to knowledge for brucellosis control among pastoral communities in north-west Côte d’Ivoire. Pastoralism. 2022; 12(1): 28.

[43] Peng R, Wang Y, Zhai J, Zhang J, Lu Y, Yi H, et al. Driving effect of multiplex factors on human brucellosis in high incidence region, implication for brucellosis based on one health concept. One Health. 2022; 15: 100449.

[44] Corbel MJ, Food and Agriculture Organization of the United Nations, World Health Organization & World Organisation for Animal Health. Brucellosis in Humans and Animals . Geneva: World Health Organization; 2006.

[45] Ma X, Sun G-Q. Global dynamics of a periodic brucellosis model with time delay and environmental factors. Appl Math Model. 2024; 130: 288-309.

[46] WAHIS (World Organisation for Animal Health). Quantitative Data Dashboard. 2024. Available from: https://wahis.woah.org Accessed on date June 25, 2024.

[47] Minas A, Minas M, Stournara A, Tselepidis S. The “effects” of Rev-1 vaccination of sheep and goats on human brucellosis in Greece. Prev Vet Med. 2004; 64(1): 41-47.

[48] Dougas G, Katsiolis A, Linou M, Kostoulas P, Billinis C . Modelling human brucellosis based on infection rate and vaccination coverage of sheep and goats. Pathogens. 2022; 11(2): 167.

[49] Khames M, Zúñiga-Ripa A, Pérez Gómez S, Oumouna M, Moriyón I. Comparison of serological tests in cattle and ovine brucellosis; an abattoir study in Algeria. World Vet J. 2020; 10(3): 457-464.

[50] Boudalia S, Boudebbouz A, Gueroui Y, Bousbia A, Benada M, Leksir C, et al. Characterization of traditional Algerian cheese “ Bouhezza” prepared with raw cow, goat and sheep milks . Food Sci Technol. 2020; 40.

[51] Hikal AF, Wareth G, Khan A. Brucellosis: why is it eradicated from domestic livestock in the United States but not in the Nile River Basin countries? Ger J Microbiol. 2023; 3(2): 19-25.

[52] Muñoz PM, Blasco J-M, Garin-Bastuji B. Brucella spp^☆ . In Encyclopedia of Dairy Sciences. 3rd edition. Edited by McSweeney PLH, McNamara JP. Oxford: Academic Press; 2022: 401-418.