Background
Brucellosis is an infectious disease of many animal species and humans caused by bacteria of the genus
Brucella [
1] and characterized by inflammation of the genitals and foetal membranes, abortions, sterility and lesions in the lymphatic system and joints [
2‐
7]. Brucellosis is an anthropozoonosis which cause great economic losses in livestock production and seriously threatens public health in countries where it is endemic [
1,
7‐
10]. Human brucellosis has been associated with acute febrile illness, severe debilitating disease that requires prolonged treatment with a combination of antibiotics, permanent disabling sequel, considerable medical expenses and loss of income due to loss of working hours [
11,
12]. Spontaneous miscarriage and in utero foetal death during the first trimesters have also been reported among pregnant women [
13]. The risks of zoonotic transmission of the disease from animals to humans are associated to climate change and corollaries of husbandry practices, eating habits and social behaviour of the populations concerned [
14].
Animal and human brucellosis is endemic and neglected in Sub-Saharan Africa [
15] due to lack of attention and absence of adequate diagnostic facilities [
14,
16], lack of public awareness, inadequate public-sector animal health services, and poor or low-income communities [
16,
17]. However, the prevalence of risk factors for infections are better understood for brucellosis in domestic ruminants particularly bovine brucellosis and this species bias is reflected in control activities [
16]. Nonetheless, the surveillance of bovine brucellosis is generally poor and mass control is difficult to implement due to the existence of conditions that favour the widespread nature and transmission of the disease in most of the region [
18,
19]. These factors include uncontrolled animal movement, migrations of pastoralists in search of pasture and water, purchase of infected cattle from livestock market for replacement or upgrading, anarchic development of urban livestock breeding and nature of the animal production system, inadequate sanitary measures, demographic factors, regulatory issues, climate, deforestation and wildlife interaction [
20‐
24].
Although there is great progress in controlling brucellosis in some countries, the disease still persists in domestic animals in many regions with frequent transmission to human populations and occurrence of human disease [
6]. The geographical distribution of zoonotic brucellosis is strongly correlated with regions where livestock is the main source of human livelihood such as food and income [
5]. Brucellosis is an important human disease in the Mediterranean countries of Europe, Africa, Middle East, South and Central Asia and Central and South America [
6,
12,
25] and yet it is neglected, underrecognized and frequently goes unreported [
6,
12,
25]. Human brucellosis is endemic in Sub-Saharan Africa and seroprevalence estimates have been reported for many countries including 3.8% in Chad [
1], 3.3% in Central African Republic, 7.7% in Tanzania [
11], 24.1% [
26] and 31.82% [
27] in Nigeria, 17% in Uganda [
28] and 1–5.6% among traditional pastoralists (Fulani) and 0–1.6% among non-pastoraalists in Togo [
15].
There is an operational and functional “One Health” National Strategy as well as a National Program for the prevention and control of emerging and re-emerging zoonoses in Cameroon. The “One Health” National Strategy evolved from the combined efforts of sectors of animal health, human health and environmental health working jointly in a trans-sectoral and synergic manner for the management of health security of animal and human population [
29]. The National Program for the Prevention and Fight against Emerging and Re-Emerging zoonoses was elaborated with the support of the RESPOND project – USAID [
30] and, in 2014, a National Program for the prevention and control of emerging and re-emerging zoonoses was enacted in Cameroon. Using inputs from the human health, livestock, environment, wildlife, research, and higher education sectors and tools developed by the U.S. Centers for Disease Control and Prevention (CDC) five priority zoonotic diseases were identified as from a list of relevant zoonoses for Cameroon including rabies, anthrax, highly pathogenic avian Influenza, Ebola and Marburg Virus disease, and bovine tuberculosis [
31]. However, poor implementation of essential control measures of zoonoses including animal brucellosis (e.g., restricting movement of infected cattle, reporting disease to the veterinary services, testing of animals) has been reported in Cameroon [
32]. Brucellosis is an important notifiable disease worldwide and there is dearth of information on the epidemiological situation of human brucellosis in the country particularly the seroprevalence of brucellosis among vulnerable communities and populations at risk including abattoir personnel and pregnant women in the Adamawa region which is the main livestock producing region of Cameroon. There are little or no concerted veterinary and medical efforts to maximize brucellosis detection rates. Active involvement of populations at risk and good health systems are lacking such that appropriate preventive measures and planning for effective control programs of brucellosis in animals and humans cannot be achieved [
33]. Bovine brucellosis is widely endemic in Cameroon and prevalence rates in the range of 3–31% in cattle at individual levels and 16.2–35.0% at herd levels have been reported [
2,
10,
22,
33‐
38]. However, determining the prevalence and risk factors of brucellosis in all livestock according to their origin could improve the epidemiology the disease in Cameroon. There are also concerns about brucellosis in other farm animals such as sheep, goats and pigs since the occurrence and epidemiology of the disease in these animals is poorly understood. Furthermore, the zoonotic potential and status of brucellosis in human communities as well as the relation between the burden and associated risk factors of brucellosis in livestock and livestock professionals in major livestock procuring zones in the country are not known.
Therefore, this study was carried out to contribute to the epidemiology of bovine and human brucellosis and estimate the seroprevalence of brucellosis in slaughtered cattle, abattoir personnel and pregnant women in Ngaoundéré Cameroon. The study also assesses the risk factors for evidence-based control of the disease in Cameroon.
Discussion
The overall seroprevalence of bovine brucellosis obtained at the Ngaoundéré municipal abattoir (3.4% for RBPT and 5.93% for i-ELISA) is different from the rates reported in other parts of the country. Though several other studies reported higher bovine brucellosis seroprevalence ranging from 7 to 31% in various parts of Cameroon [
22,
33‐
38,
53], lower seroprevalence rates have been recorded in indigenous cattle such as 3% using competitive ELISA [
37] in Adamawa Region and 4.6% with RBPT in Northwest region [
36]. The results obtained in this study is similar to various serological findings reported in indigenous cattle farming systems in Niger (1.3%) [
54], Ivory Coast (4.6%) [
55], Nigeria (3.9%) [
24], Chad (2.6%) [
1,
56], Central Africa Republic (3.3%) [
57], Uganda (3.3%) [
58], Zimbabwe (5.6%) [
59,
60], and Ethiopia (2.4–3.9) [
23,
61,
62] as well as in the municipal cattle slaughterhouse (4.88 and 5.82%) in Ibadan Nigeria [
27]. However, higher rates have been reported in Ivory Coast (8.8–10.3%) [
63,
64], Zambia (18.7%) [
20], Mali (22%) [
65], Burkina Faso (13.2%) [
66], and Algeria (9.7%) [
67]. The differences in prevalence rates reported in Cameroon and other parts of Africa could also be associated with the evolution of the disease, geographical origin, breeds, sample size, study frame as well as the protocol adopted such as the type and number of diagnostic tests used. The protocol could have involved one test or more than one test in series (screening test followed by confirmation of positive reactors by another test) or in parallel (all tests are applied on the sampled animals independently) [
33,
55,
63,
68‐
70]. Furthermore, close antigenic cross-reactivity with other bacterial infections
(Yersinia,
Xanthomonas,
Salmonella,
Streptococci,
E. coli, tuberculosis) can lead to false positive results being encountered in serological diagnosis of brucellosis [
71,
72].
The study observed that breed was the major factor for high bovine brucella seropositivity compared to sex, age, body condition score and state of gravidity of the animals that had no significant influence on the seroprevalence. The finding is similar to Akinseye et al. [
24] and Ojong [
36] who did not observe differences in seropositivity due to sex. It is contrary to Ojong [
36] who reported difference due to breed and Awah-Ndukum et al., [
33] who reported differences due to age and sex and not by breeds and body condition score. Though level of susceptibility of breed to brucellosis was not ascertained by the study, the difference observed are associated to the ethnic groups of pastoral communities have different behaviours in conducting and systems of keeping their livestock. The Djafoun and Akou cattle in this study are kept by the Mbororo / Fulani ethnic groups who predominantly associate transboundary animal movements, migrations and transhumance to their husbandry activities compared to the Foubles who keep Gudali cattle and are generally sedentary. Domenech et al., [
2] found a brucellosis seroprevalence ranging from 15 to 40% in cows in pastoral/agropastoral systems in Chad and Cameroon, which mixed up all animals (pregnant or not) compared to brucellosis seroprevalence of 8.5% in cattle of a particular tribe / ethnic group who kept their cattle in small herds during the rainy season and grouped all the animals together during the dry season to move to graze land with the exception of pregnant animals which remained in the village. Also, the major source of variation for brucellosis prevalence in the of risk of different diseases was observed between-farm [
73], suggesting that cattle herd management practice within production systems could be more important factors than the mainly environmental variables used for differentiating between the systems [
2,
74]. General poor condition of animals [
75], aging and high parity [
3,
4,
14,
34,
66,
76] have been observed to significantly increase bovine brucellosis seroprevelance. In addition, animals become more sensitive to brucella infection at reproductive age [
34,
76,
77].
Though brucellosis occurs naturally in animals, the human disease has been reported especially in regions where bovine brucellosis is endemic [
6] and its prevalence in humans tends to correspond to that in animals [
6,
28,
78]. In the present study, the overall brucellosis seroprevalence among abattoir personnel (5.6%) is comparable to the overall seroprevalence of bovine brucellosis at the abattoir (3.4%) and 3% rate earlier reported in live animals using complement ELISA [
37]. However, Brucella IgG ELISA brucella seropositivity (12.15%) among abattoir personnel was significantly higher than i-ELISA brucella seropositivity (5.93%) in the abattoir cattle. The high Brucella IgG ELISA human seroprevalence parallels with bovine brucellosis seroprevalence (RBPT, i-ELISA, competitive ELISA) reported in the study region and other parts of Cameroon which ranged from 7 to 31% in live cattle [
33‐
35,
38]. The seropositive humans (> 66.67%) presented > 200 U/ml IgG concentrations and also reported febrile illnesses, body weakness, sweating, painful joints and muscular pains. Seropositive pregnant women in the study regularly consume raw milk and had history of exposure to aborted animal foetuses and previous miscarriages. Brucellosis patients have been associated with significantly elevated levels of
Brucella IgG and differentiation between brucellosis from non-brucellosis patients have been done by measuring
Brucella IgG concentrations [
79]. The finding of
Brucella IgG seropositive humans with milder clinical symptoms and < 50 U/ml serum
Brucella IgG concentrations might be due to a long-ago infection with the
Brucella IgG level waning / decreasing over time and lack of further exposure to infection or source of infection. Sippel et al. [
79] stated that ELISA was excellent for screening populations for anti-
Brucella antibodies and differentiating between phases of the disease and reported high levels of blood IgG which lasted up to 8 months following persisting
Brucella infections. It is worth noting that these non-specific symptoms (fatigue, myalgias, arthralgias, headaches, chills) are shared by much more prevalent tropical diseases such as malaria [
25,
80].
This study presents the first of human brucellosis seroprevalence report from Cameroon and the infected animals in the study area probably serve as reservoirs and sources for the human brucellosis recorded. Therefore,
Brucella infection is an important public health problem in Cameroon since traditional pastoral and agropastoral communities are widespread with the inhabitants depending almost entirely on livestock for livelihood. The brucellosis seroprevalence (5.6% [5.6% for RBPT, 12.15% for Brucella IgG ELISA]) among abattoir personnel recorded in this study is lower than rates ranging from 10 to 17% among abattoir workers, livestock rearing communities and individuals with febrile illnesses in hospital in Uganda [
28,
81,
82], 21.2% among patients with febrile clinical signs, 24.1% among abattoir workers and 44% among butcher workers in Nigeria [
26,
83,
84], 40% among pastoralists in Libya [
85] and 8% in pastoral communities following implementation of relevant control measures in Egypt [
86]. Human brucellosis seroprevalence was usually high among livestock professionals, people who live in pastoral communities, habitually consume raw milk and milk products, in addition to processing milk products [
6,
26,
28,
81‐
88].
This study showed that the human brucellosis seroprevalence varied among the categories of abattoir personnel, suggesting further investigation. Age, poor educational level and longevity of service were associated with slight increase in seroprevalence. Female personnel were brucella seronegative and seropositivity was highest among butcher apprentices who handled foetuses and clean offal, followed by meat sellers and butchers whose main job was slaughtering of animals. Though all seropositive abattoir personnel did not wear protective equipment at work and potential factors were associated with non-significantly higher human brucellosis seroprevalence including consuming raw milk, handling foetuses, occupational exposure of over 5 years, knowledge of brucellosis, owning and contact with livestock outside the abattoir and home environments. However, it should be noted that abattoir personnel in the study were muslim-dominated and may have accounted for the absence of contact between seropositive reactors and pigs. The study revealed that butcher apprentices who handled foetuses and uterine contents were more at risk compared to the other occupational groups probably due of their close contacts with infected blood and tissues of infected animals as well as infected foetuses and uterine contents. Several reports in Nigeria, Tanzania and Egypt have highlighted that among occupational groups in abattoirs, seroprevalence of brucellosis was highest among butchers whose main job was slaughtering of animals, followed by livestock traders, meat sellers and abattoir cleaners compared with the other workers [
26,
27,
89,
90]. Also, transmission of human brucellosis by inoculation through cuts and abrasions in the skin [
6,
91] and increase of brucellosis seroprevealence among butchers with injuries slaughtering animals compared to other abattoir workers [
26] have been reported.
In agreement with the finding of Aworh et al., [
26], veterinarians and para-veterinarians, considered to be at high occupational risk, were not found to be
Brucella seropositive in this study. This may be attributed to their awareness of the zoonotic brucellosis and the use of personal protective equipment and short exposure time of veterinarians at the abattoir during meat inspection coupled with good personal hygiene practices during work. Short exposure time and good personal hygiene practices may also be associated to the
Brucella seronegative reactions observed among the administrative staff and abattoir visitors (cattle owners and cattle traders that visited the abattoir, restaurant vendors at the abattoir to purchase meat).
There was no statistically significant correlation between human brucellosis seroprevalence and contact with home-owned animals, assisted animal parturitions, slaughter of animals, and contact with domestic animals. However, these findings are contrary to previous reports that the occurrence of human brucellosis was associated with contact with domestic animals [
92], exposure to aborted animals and assisting animal parturition [
93‐
95] and or sharing of water sources with animals [
96]. Similar to the findings of Tumwine et al., [
28], this study largely depended on self-reporting by the participants who could have left out some potential factors associated to zoonotic brucellosis as more seropositive respondents had no knowledge of the disease.
The study used serological tests (RBPT and ELISA) in combination to minimize measurement of false positive errors and revealed that human brucellosis is a real public health problem in Cameroon. No significant association was observed for human brucellosis seropositivity regarding drinking of milk (raw and pasteurized) and knowledge of zoonotic brucellosis (Yes and No). However, emphasizes should be on the importance of drinking only pasteurized milk and sensitization of animal professionals to improve their level of awareness, as the outcome might have been due of the subject group used in the study. Therefore, it is more likely that human brucellosis seroprevalence would be higher in communities where people live among livestock since bovine brucellosis is reported to be highly endemic in the country [
22,
33‐
38].