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AIMS Microbiology, 10(1): 1–11.
DOI: 10.3934/microbiol.2024001
Received: 18 September 2023
Revised: 11 December 2023
Accepted: 20 December 2023
Published: 02 January 2024
http://www.aimspress.com/journal/microbiology
Research article
Seroprevalence of brucellosis among animal handlers in West
Bengal, India: an occupational health study
Dolanchampa Modak1,†, Silpak Biswas1,†, Agnibho Mondal1, Malabika Biswas1,*, Maria
Teresa Mascellino2, Banya Chakraborty1, Simmi Tiwari3, Ajit Dadaji Shewale3, Tushar
Nale3 and Rupali Dey1
1 Department of Microbiology, School of Tropical Medicine, Kolkata 700073, India
2 Department of Public Health and Infectious Diseases, Sapienza University of Rome, Rome 00185,
Italy
3 Centre for One Health, National Centre for Disease Control (NCDC), Ministry of Health & Family
Welfare, Delhi 110054, India
†These two authors contributed equally to this work.
* Correspondence: Email: mb7081@gmail.com.
Abstract: Brucellosis is a highly contagious zoonotic disease and a major human health problem
worldwide. Due to its ways of transmission, direct or indirect contact with infected animals or their
contaminated biological products, the disease exhibits strong occupational association with animal
handlers comprising a significant population at risk. This study was undertaken to estimate the
seroprevalence of brucellosis in animal handlers and to understand the epidemiological and
serological aspects of the same. The animal handlers from the state of West Bengal, India were
included in this study. It was a prospective and observational cohort study from November 2021 to
March 2022. A total of 669 sera samples were collected from animal handlers and tested using
various serological tests for Brucella antibodies. All serum samples were tested using the Rose
Bengal plate test (RBPT), standard tube agglutination test (STAT), and enzyme-linked
immunosorbent assay (ELISA). 106 (15.8%) patients were diagnosed with brucellosis among the
total number of patients tested. Most of the patients affected with brucellosis belonged to the age
group 51–60 years (23.5%). The seropositivity rate in male animal handlers was higher than female
animal handlers in this study. More studies are needed to understand the occupational association of
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this disease. Awareness programs, safe livestock practices, and prevention of the disease by timely
diagnosis must be implemented in order to control human brucellosis.
Keywords: Zoonotic disease; brucellosis; animal handlers; seroprevalence
1. Introduction
Brucellosis is one of the most common zoonotic diseases worldwide. Brucellosis is caused by a
Gram-negative coccobacilli belonging to the genus Brucella (family Brucellaceae) [1–5]. Among the
prevalent species, Brucella melitensis, Brucella abortus, Brucella suis and Brucella canis are
pathogenic to humans [6,7]. In humans, the disease is characterized by a variety of manifestations
including fever, night sweats, myalgia, arthralgia, and weakness [8]. The wide spectrum of clinical
manifestations and the lack of pathognomonic symptoms make human brucellosis difficult to
clinically diagnose and distinguish from several febrile conditions that often occur in the same areas.
Therefore, laboratory tests are essential for diagnosing the disease. Brucellosis is associated with loss
of livestock productivity and trade, thus incurring massive economic losses [9].
In spite of successful eradication attempts in many countries around the world, brucellosis exists
as a potent animal and human health issue in developing as well as in developed countries [10]. In
developed countries, it is prevalent in wild animals and can be a threat due to spill-over infection
potential. Brucellosis is considered an endemic disease in India [9]. Many Indian people have close
contact with domestic animals because of their occupation, particularly those involved in agriculture.
Therefore, they have an increased risk of contracting many zoonotic diseases including brucellosis [11].
A study by Shukla et al. [12] in different Indian states showed that the overall seroprevalence of
brucellosis from tertiary care health settings was 11% (772/7026). The majority of positive cases
were from the states of Madhya Pradesh (58.1%), Maharashtra (38.8%) and Chhattisgarh (2.9%).
Adults and females were more vulnerable among the study population [12]. Dutta et al. [13]
investigated the presence of childhood brucellosis cases in Eastern zone of India. The findings from
this study revealed the higher percentage of infection in female children (14.3%) than in male
children (10.9%) [13]. Seroprevalence of 8.5% was reported in dairy workers by Mathur in their
older study [14]. Looking at studies over time (from 1986 to 2011) there was wide variation of the
prevalence of human brucellosis in India, such as 0.8% in Kashmir, 6.8 % in Varanasi, 8.5% in
Gujarat, 11.51 % in Andhra Pradesh, 19.83% in Maharashtra, and 26.6 % in Ludhiana [15–20]. It is
estimated that less than 10% of cases of human brucellosis are recognized and treated in India [21]. A
recent rise of the disease in this country has been attributed to intensified developments in the dairy
industry resulting in increased livestock population [9]. A high seroprevalence of anti-Brucella
antibodies has been noted among veterinarians and veterinary pharmacists [22] in previous studies.
Along with veterinary professionals, animal handlers comprise a significant population at risk of
contracting brucellosis due to their continued involvement in health and management of livestock.
In India, the veterinary services fall under the purview of the state government. Most of the
states have three types of veterinary health care workers: (1) qualified registered veterinarians, (2)
paraveterinarians, and (3) animal handlers [23]. The animal handlers are engaged in artificial
insemination, vaccination, and deworming of cattle [24] as part of veterinary services. They are
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consequently exposed to all possible routes of transmission of Brucella spp. including contact with
secretions of diseased animals and needle stick injuries while vaccinating female calves. Handling of
potentially infected animals, contaminated biological materials, and live attenuated anti-brucellosis
vaccines are risk factors for human brucellosis. However, more detailed knowledge about particular
risk factors to each occupation, as well as the measurement of these risks is still scarce. In fact, there
is a need for more accurate data on the epidemiology of job-related brucellosis to allow the
implementation of more effective preventive measures, which will reduce the impact of the disease
in groups exposed by their work activities.
There are presently three live Brucella vaccines available commercially: B. abortus strain 19 (S19),
B. abortus strain RB51 (RB51), and B. melitensis strain Rev 1 (Rev1) in animals [25]. Among these
vaccines, S19 is most commonly used in all vaccination programs in India. It is a modified live
culture vaccine [25]. However, Brucella vaccines have been documented to cause human brucellosis
if accidental exposure occurs [26].
In India there exists a dearth of studies documenting brucellosis in animal handlers associated
with vaccination program. Therefore, the objective of the present study was to (1) estimate the
prevalence of brucellosis in animal handlers accidently exposed to S19 vaccine and (2) understand
the epidemiological and serological aspect of the same. The serodiagnosis of brucellosis is mostly
based on consensual criteria such as given titer in agglutination assay, a cut-off ELISA reading value,
etc. Furthermore, the sensitivity and specificity of any serological test for brucellosis depends highly
among other factors, on local epidemiological conditions [27]. The results of serological tests for
brucellosis require interpretation that is often difficult and inconclusive [28]. Therefore, at least two
positives out of three serological tests were used as criteria for diagnosis of brucellosis in
surveillance in this study [29].
2. Materials and methods
2.1. Study design and study population
It was a prospective and observational cohort study conducted by the School of Tropical
Medicine, Kolkata, India from November 2021–March 2022. The study was done by the Department
of Microbiology and Department of Tropical Medicine and was supported by National One
Health Program for Prevention and Control of Zoonoses (NOHP-PCZ), National Centre for
Disease Control (NCDC), Delhi, India. The target population included animal handlers from the
state of West Bengal, India, with a history of accidental exposure to Brucella abortus vaccine (S19
strain). An accidental exposure was defined as a needle stick injection through the skin or sprays or
splash into the eye or broken skin of a human while handling the S19 vaccine [30].
2.2. Sample collection
Blood samples (2 mL) were collected from animal handlers reporting to the Outpatient
Department of the School of Tropical Medicine (Kolkata) from various districts of West Bengal.
Information regarding age, sex, geographic location, type of animal handling activity, history of
exposure, clinical history, and other relevant details was obtained after seeking consent from the
patients.
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2.3. Criteria for positive diagnosis of brucellosis
(a) History of association with animals, with or without symptoms like fever, joint pains, chills,
body ache and (b) detection of anti-Brucella antibodies by at least 2 serological tests [29] in
significant titers (≥1:160 in case of STAT) [31].
2.4. Methods
Serum was separated from blood samples by centrifuging at 3000 rpm for 5 minutes. The
samples were stored at 4 ℃ until further testing. All serum samples were tested using three
serological tests: the Rose Bengal plate test (RBPT), standard tube agglutination test (STAT), and
enzyme-linked immunosorbent assay (ELISA).
2.4.1. RBPT
The RBPT is a spot agglutination test. In this test, 30 µL of B. abortus S99 colored antigen and
30 µL of patient serum was taken on a clean glass slide and mixed well. The test was interpreted as
negative when agglutination was absent. When agglutination was present, the test was interpreted as
positive and rated from 1+ to 3+. This was according to the strength of the agglutination observed
from 1–3 minutes [29]. For RBPT, B. abortus S99 colored antigen was procured from Indian
Veterinary Research Institute (IVRI, Bareilly), Uttar Pradesh, India.
2.4.2. STAT
For the standard tube agglutination test (STAT), two-fold serial dilutions of the serum samples
were prepared from 1:20 to 1:320 according to the Weybridge technique. The highest dilution of the
serum exhibiting mat formation was considered as end point titer. A titer of 1:160 and above was
considered significant for human brucellosis [29,31].
2.4.3. ELISA
Indirect ELISA testing for anti-Brucella IgM was performed using a commercially available
ELISA kit (NOVALISA, NOVATEC, Germany). The indirect ELISA method was used because of
its high sensitivity. The test was performed and results were interpreted as per kit literature.
2.5. Ethical statement
The study was approved (approval number: 2022-AS3) by Institutional Ethics Committee,
School of Tropical Medicine, Kolkata, India.
2.6. Statistical analysis
The data obtained in this study was analyzed by R version 4.3.2 by R Foundation for Statistical
Computing.
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3. Results
In the present study, a total of 669 sera samples were collected from animal handlers and tested
using three serological tests (RBPT, STAT, ELISA) for Brucella antibodies. Of these, 106 (15.8%)
were diagnosed with brucellosis according to the pre-determined criteria. Among the total number of
samples collected, 312 (46.6%) were males and 357 (53.4%) were females. Among those who were
seropositive, 53 were male and 53 were female (Table 1). It is interesting to note that 99.7% (310 out
of 311) of artificial insemination workers (AI workers) were males.
Table 1. Number and percentage of seropositivity in males and females found in this study.
Sex
Total Samples Collected
Seropositivity (N %)
Males
312
53 (17%)
Females
357
53 (14.8%)
Most of the samples were collected from the age group of 31–40 years (n = 362) followed by 41–50
years (n = 153). The largest percentage of seropositivity was noted in the age group of 51–60
years (23.5%). In this study, 8.8 % seropositivity was found in the age group of 21–30, 14.9% in the
age group of 31–40, and 20.3% in the age group of 41–50 (Table 2).
Table 2. Table showing percentage of seropositivity in different age groups of animal handlers.
Age group (in Years)
Total Samples Collected
Total Samples Seropositive (N %)
<20
3
0 (0%)
21-30
90
8 (8.8%)
31-40
362
54 (14.9%)
41-50
153
31 (20.3%)
51-60
51
12 (23.5%)
>60
10
1 (10%)
Regarding district-wise distribution, the largest number of samples were collected from patients
from the district of Nadia (166), followed by North 24 Parganas (83), and Bankura (82) of West
Bengal. Only one sample was collected from Jhargram and Medinipur district. Among these, the
sample from Jhargram was positive and the sample from Medinipur was negative. Among the two
samples collected from the Malda district, one was positive and two out of four samples from
Paschim Burdwan were positive. Other districts of West Bengal, such as Purba Medinipur (47.6%),
Murshidabad (42.4%), Purba Burdwan (26.4%), displayed higher percentages of seropositivity (Table3).
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Table 3: Total seropositivity found in different districts of West Bengal, India.
Districts of West Bengal
Total Samples Collected
Total seropositivity in each district
Bankura
Birbhum
Burdwan
Cooch Behar
Hooghly
Howrah
Jhargram
Malda
Medinipur
Murshidabad
North 24 Parganas
Nadia
Purba Burdwan
Paschim Burdwan
Paschim Medinipur
Purba Medinipur
Purulia
South 24 Parganas
Uttar Dinajpur
Unknown
82
24
4
4
30
25
1
2
1
33
83
166
34
4
21
21
2
32
38
62
13 (15.8%)
2 (8.3%)
0
1 (25%)
5 (16.6%)
1 (4%)
1 (100%)
1 (50%)
0
14 (42.4%)
15 (18%)
19 (11.4%)
9 (26.4%)
2 (50%)
4 (19%)
10 (47.6%)
0
4 (12.5%)
2 (5%)
3 (4.8%)
3.1. Analysis of serological tests
Among the total number of tests performed, RBPT showed positive results in 124 (18.5%) patients.
Only RBPT showed a positive result for three (0.4%) of the patients. However, significantly high
STAT titers were found in 104 (15.5%) patients. All three tests showed positive results in 91 (13.6%)
patients, while two out of the three tests (RBPT and SAT) showed positive results in 13 (1.9%)
patients (Table 4).
Table 4: Results of serological tests (RBPT, SAT, and ELISA).
RBPT
SAT
ELISA
N (%)
+
+
+
91 (13.6%)
+
+
-
13 (1.9%)
-
-
-
535 (79.9%)
+
1:80
-
17 (2.5%)
+
-
-
3 (0.4%)
The overall prevalence of seropositivity was found to be 15.8% (95% confidence interval 13.2
to 18.8). It was not significantly different from the previously reported prevalence of 11% by Shukla
et al. [12] with a p value of 0.89. Seropositivity has no association with age (p = 0.22), sex (p = 0.45),
type of animal handler (p = 0.32), or mode of exposure (p = 0.13).
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4. Discussion
Brucellosis, which is one of the neglected zoonotic diseases with economic importance, is either
misdiagnosed or underreported in many parts of the world. Brucellosis has a strong occupational
association, with certain professions being more commonly affected by the disease [22]. The disease
can lead to serious complications in affected patients with an important public health issue.
Even though the continent of Asia comprises 60% of the world’s population with India
forming 17%, there are lacunae of studies reporting human brucellosis [9,32]. There are studies on
the concurrent existence of human and animal brucellosis exploring the epidemiology of this disease
in veterinary professionals [22,33–35]. However, to the best of our knowledge, there is no study
documenting human brucellosis due to possible accidental exposure to the S19 vaccine in the Indian
subcontinent. The present study provides valuable insights into occupational brucellosis. A study by
Pereira et al. [36] in Minas Gerais, Brazil gives a detailed insight into accidental exposure to S19 and
RB51 vaccines. The study revealed that one-third of the interviewed professionals had been
accidentally exposed to the vaccine [36].
In the present study, routine serological tests (RBPT, STAT, and ELISA) have been used for the
diagnosis of brucellosis. Here, among 669 animal handlers, 106 (15.8%) were diagnosed with
brucellosis. The overall prevalence of seropositivity of 15.8% (95% confidence interval 13.2 to 18.8)
was not significantly different from the previously reported prevalence of 11% by Shukla et al. [12]
with a p value of 0.89. Previously, a high prevalence of occupational brucellosis was found in animal
handlers (16.12%) demonstrated by Shome et al. [29], and this was in accordance with our findings.
It may be inferred that the lack of knowledge about brucellosis and protective measures among
animal handlers increases the probability of infection. The seropositivity distribution observed in
males and in females was 17% and 14.8%, respectively (Table 1). This was higher compared to the
data reported by Shome et al. [29], where they found 7.45% of males showed seropositivity and none
of the females showed seropositivity. In our study, most of the samples were collected from the age
group of 31–40 years. However, the highest rate of seropositivity was noted in the age group of 51–60
years (23.5%). The seropositivity was found to be 8.8% in the age group of 21–30, 14.9% in the age
group of 31–40, and 20.3% in the age group of 41–50 (Table 2). In this study, the percentage of
seropositivity was higher in the age groups of 31–40 and 41–50, compared to the previous study by
Shome et al. [29]. High brucellosis seroprevalences were observed in the age groups 21–30 (8.90%),
41–50 (7.85%), and 31–40 (6.75%) by Shome et al. [29]. Regarding districts-wise distribution, the
largest numbers of samples were collected from the district of Nadia (166), followed by North 24
Parganas (83) and Bankura (82) of West Bengal. We found variation in the seropositivity rate among
the different districts. Statistical analysis showed that seropositivity has no association with age (p = 0.22),
sex (p = 0.45), type of animal handler (p = 0.32), or mode of exposure (p = 0.13).
Human brucellosis has been reported earlier among pyrexia of unknown origin (PUO) cases,
animal handlers, veterinarians, and slaughterhouse workers in India in some hospital based
surveillance studies and case reports [37–41]. Our study concurs with the findings of similar studies
on accidental exposure to the S19 or RB51 vaccine, where more than half of the target population
recalled needle stick injuries [23,42]. Vaccine bottle opening, syringe capping and recapping, and
poor infrastructure were all significant risk factors of acquiring the disease. A study by Proch et al. [24]
in India found more occupational brucellosis in veterinary assistants than among veterinarians. In our
study, we have solely documented the disease in a cohort of animal handlers with relevant exposures.
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The slow growth of Brucella in primary cultures delays diagnosis. Therefore, serological tests
play a major role in the routine diagnosis of brucellosis [27,43]. This was evident in our study when
the initial 54 blood cultures of symptomatic patients showed no growth. Most of the diagnostic
methods currently used for human serological testing use as antigen, whole “smooth” Brucella cells,
or bacterial extracts containing high concentrations of sLPS [25]. Serological tests have problems of
false positivity and negativity [27,44]. Therefore, our study reiterates the fact that a single diagnostic
test cannot be used to arrive at a diagnosis of human brucellosis.
Post exposure antibiotic prophylaxis has been recommended for humans accidentally exposed
to anti-Brucella vaccines [45]. Based on literature on adverse events linked with vaccination
campaigns, it is recommended that those concerned with the administration of this vaccine should
wear gloves and eye protection to minimize exposure [26]. In spite of several efforts, the true burden
of endemic brucellosis in our subcontinent remains to be seen. As there were no positive growths
found in the blood cultures in this study, it could not be concluded if B. abortus strain 19 (S19) was
responsible for brucellosis in the animal handlers. Therefore, more studies of human and animal
brucellosis across the country are needed to distinguish between the transmission of the disease as a
zoonotic disease and its transmission by other routes.
5. Conclusion
Brucellosis is a neglected disease whose problems are underreported worldwide, particularly in
South Asia and India. Accidental exposure to the live S19 Brucella vaccine poses a significant threat
to animal keepers in the Indian subcontinent. This study showed a seropositivity rate of 15.8%
among Indian animal workers, suggesting a lack of awareness and protective measures among them.
Female handlers had a seropositivity rate of 14.8%, while the rate of seropositivity for males was 17%.
The highest seropositivity was found in the 51- to 60-year-old age group (23.5%). Recommendations
include increased awareness, surveillance, improved safety measures through animal handler training,
and prioritization of robust diagnostic tests like RBPT both in animals and humans. Moreover,
animal brucellosis eradication programs needed to be implemented in order to control human
brucellosis since the transmission is zoonotic.
Acknowledgements
Authors thank the technical assistance of Indian Council of Agricultural Research-National
Institute of Veterinary Epidemiology and Disease Informatics (ICAR-NIVEDI), Bengaluru, India.
Conflicts of interest
Maria Teresa Mascellino is an editorial board member for AIMS Microbiology and was not
involved in the editorial review or the decision to publish this article. All authors declare that there
are no competing interests.
Author contributions
Dolanchampa Modak, Silpak Biswas, Malabika Biswas: Conceptualization, Methodology,
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AIMS Microbiology Volume 10, Issue 1, 1–11.
Investigation and Writing Original Draft, Data curation, Formal Analysis, Writing Review and
Editing; Agnibho Mondal: Data curation and Formal Analysis; Maria Teresa Mascellino: Validation,
Writing Review and Editing; Banya Chakraborty, Simmi Tiwari, Ajit Dadaji Shewale, Tushar Nale,
Rupali Dey: Conceptualization, Supervision, Project Administration, Validation, Writing Review
and Editing.
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