Seroprevalence of Brucellosis in Camels in Sindh, Pakistan

Abdul Sattar Baloch 1*, Abdul Rasheed 1,2, Rahmatullah Rind 1, Jam Kashif Sahito 1, Rehana Buriro 1, Muhammad Faisal Ayoob 1 and Parkash Dewani 1

1Faculty of Animal Husbandry and Veterinary Sciences, Sindh Agriculture University, Tandojam 70050, Pakistan

2South Bohemian Research Center for Aquaculture and Biodiversity of Hydrocenoses, Research Institute of Fish Culture and Hyrdrobiology, Faculty of Fisheries and Protection of Waters, University of South Bohemia in Ceske Budejovice, Zatisi 728/II, 389 25 Vodnany, Czech Republic

ABSTRACT

Brucellosis affects a wide range of animal species including human beings and is more severe in human than in animals. It imposes a huge burden on human health due to its zoonotic nature. Our study involves the testing of 100 sera samples and 50 milk samples from camels of three districts of Sindh province of Pakistan. Rose Bengal Plate Test (RBPT), serum agglutination test (SAT) and competitive-ELISA (c-ELISA) were used as screening tests, and overall seroprevalence of brucellosis was found to be as 21%, 21% and 13% by RBPT, SAT and c-ELISA tests, respectively. Seroprevalence was higher in females (26%) than in males (16%) by RBPT and SAT tests, and also in camels less than 9 years of age (13.33%). Milk samples were collected to detect the antibodies against the disease, however, none of the sample was found to be positive for brucellosis. It was concluded that the brucellosis is prevalent among camels of studied areas.

Article Information

Received 27 January 2016

Revised 12 April 2016

Accepted 23 April 2016

Available online 28 November 2016

Authors’ Contributions

RR, JKS, ALB, RB designed the study. ASB, AR, PD and MFA executed the experimental work. PD and AR wrote the article.

Key words

Brucellosis, Camels, Zoonosis.

* Corresponding author: baloch.rasheed@hotmail.com

0030-9923/2017/0001-0391 $ 9.00/0

Copyright 2017 Zoological Society of Pakistan

DOI: http://dx.doi.org/10.17582/journal.pjz/2017.49.1.sc5

B rucellosis is a notorious disease affecting a wide range of animal species including human beings, and caused by the genus Brucella (Moreno and Moriyón, 2002). The causative agent is transmitted vertically or horizontally under normal conditions, due to close contacts like sexual intercourse, secretions and by licking the aborted fetuses. Brucellosis is more severe in human beings than in domestic animals producing different clinical symptoms, just like debilitating chronic flu with illness (Dalrymple-Champneys, 1960; Pedro-Pons et al., 1968), while in animals it causes abortion, infertility and decreased milk production (Hegazy et al., 2011). Due to its zoonotic nature it imposes a huge global burden on human health and animal productivity (WHO, 2005). Studies have shown that greatest risk of transmission of this disease is mainly associated with indirect contact with animals (consumption of unpasteurized milk/dairy products). Products from sheep and goat presented more risk than the camels and cattle, and this disease also transfers through assisting animals in parturition (Cooper, 1992; El Sherbini et al., 2007).

The ruminants infected with the Brucella spp. are known to be primary source of human infection (Marcotty et al., 2009). Furthermore prevalence of human brucellosis has increased in Middle Eastern and central Asian countries, especially in Syria, Saudi Arabia, Iraq, Iran and Turkey with annual incidence rates of 160, 21, 28, 24, and 26 cases per 100,000 persons-years at the risk, respectively (Pappas et al., 2006).

According to the OIE, the brucellosis accounts 500,000 human cases per annum, thereby making it the second most important zoonotic disease (Pappas et al., 2006). Sero-prevalence of Brucella abortus was described few years back in the cattle and buffaloes in Pakistan (Ali et al., 2013). Brucella melitensis and Brucella abortus cause brucellosis in camels, and it is also difficult to diagnose brucellosis in camels since these organisms provoke only few clinical signs.

Camels are the prime source of meat and milk in many desert areas of world and Pakistan (Ali et al., 2009). Present study is a cross-sectional survey on seroprevalence of brucellosis in Sindh province of Pakistan.

Materials and methods

Three main districts of Sindh province i.e., Thatta, (Latitude 24° 47’ North, Longitude 67° 23’ East) Badin (Latitude 24° 5’ to 25° 25’ North, Longitude 68° 21’ to 69° 20’ East) and Tharparkar were selected in 2013 to determine the seroprevalence of Brucella infections in camels and also to identify potential risk factor associated with seropositivity.

A total of 100 blood samples were collected and kept in refrigerator overnight for reparation of serum which was used for Rose Bengal Plate Test (RBPT) according to Gabbar (1992), serum agglutination test (SAT) and competitive-ELISA (c-ELISA) tests. In latter test a strong positive sample showed a clear transparent appearance while, the negative sample appeared orange.

A total of 50 milk samples collected from lactating female camels were used for Milk Ring Test (MRT) according to Gabbar (1992).

Results and discussion

A total of 100 serum samples, 50 each from males and females were collected and examined through RBPT, SAT and c-ELISA; 21, 21 and 13 sera were found positive for brucellosis, respectively, by these tests. The highest prevalence of brucellosis was found in Tharparker detected by all used serological tests. High prevalence of brucellosis might be due to free moving and grazing on open pastures and close contacts with infected animals. Secondly, the proper treatment is not provided to the infected animals.

In our present study we found higher prevalence of brucellosis in camels, which is not consistent with results of other study in which lower prevalence (9.26%) was recorded (Fathey and Moghney, 2004), and is consistent with other studies (11.42) (Junaidu et al., 2006; Mukhtar and Kokab, 2007). Highest prevalence of brucellosis was detected in camels by RBPT and SAT, however, there are chances of false positive due to cross reaction with antibodies of other bacterial species whereas the c-ELISA is more reliable than two aforementioned tests. This difference in seroprevalence might be due to parity, breed, managemental and seasonal variations or might be problem in recording the observation during investigation. Such kind of cross-sectional study was also conducted in Ethiopia and the overall prevalence of brucellosis was recorded as 11.9% by RBPT and 7.6% by CFT (Complement Fixation Test), and it was concluded that camel brucellosis was widely distributed in districts of Afar province. However, Sisay and Wereta (2012) found lower prevalence of camel brucellosis in Ethiopia, while in our study prevalence was higher, but seroprevalence determined in camels of Badin district by various techniques is similar to seroprevalence of brucellosis recorded in camels of two districts of Ethiopia through RBPT. Hence, results regarding seroprevalence in three districts of Sindh are in similar pattern as demonstrated in Ethiopia.

The prevalence of brucellosis was detected in 26% females and in 16% males by RBPT and SAT, however lower prevalence of brucellosis was found in males (10%) and females (16%) camels by c-ELISA (Table I). It was found that the prevalence of brucellosis in females were higher than that of males. It might be due to opening of cervix during estrus for more than a week, gets infected with brucella spp.

The prevalence of brucellosis in females and males was 26% and 16%, respectively. We found that prevalence of brucellosis in females was higher than in males, suggesting that females are at high risk of brucellosis than males. This is consistent with study of Ismail et al. (2012) as their study found that a higher seroprevalence of brucellosis (38.5%) was observed in adult females having the history of reproductive problems such as abortion, still birth and retained fetal membrane. However, no statistically significant difference was recorded in the study of Bekele et al. (2013); hence their findings are not in the agreement with our study and findings of Adamu and Ajogi (1999) and Junaidu et al. (2006).

Table I shows higher prevalence of brucellosis in camels less than 9 years of age, while lower prevalence was recorded in camels above 10 years of age. Higher prevalence of brucellosis in camels under 9 years of age might be due to lesser immunity.

Table I.- Brucellosis positive samples from blood samples of animals of different genders and age groups from Thatta, Badin and Tharparkar districts of Sindh.

A. Different districts | RBPT | SAT | c-ELISA
Thatta |  |  |
No. of samples examined | 33 | 33 | 33
Positive samples No. (%) | 6 (18.18%) | 6 (18.18%) | 2 (6.06%)
Tharparker |  |  |
No. of samples examined | 34 | 34 | 34
Positive samples No. (%) | 11 (32.35%) | 11 (32.35%) | 8 (23.0%)
Badin |  |  |
No. of samples examined | 33 | 33 | 33
Positive samples No. (%) | 4 (12.12%) | 4 (12.12%) | 3 (9.09%)
B. Different genders |  |  |
Females |  |  |
No. of serum samples | 50 | 50 | 50
Positive samples No. (%) | 13 (26.0%) | 13 (26.0%) | 8 (16.0%)
Males |  |  |
No. of serum samples | 50 | 50 | 50
Positive samples No. (%) | 8 (16.0%) | 8 (16.0%) | 5 (10.0%)
C. Different age groups |  |  |
Age under 9 years |  |  |
No. of serum samples | 60 | 60 | 60
Positive samples No. (%) | 17 (28.33%) | 17 (28.33%) | 8(13.33%)
Age above 10 years |  |  |
No. of serum samples | 40 | 40 | 40
Positive samples No. (%) | 4 (10.0%) | 4 (10.0%) | 5 (12.5%)

RBPT, Rose bengal plate test; SAT, Serum agglutination test; C-ELISA, competitive ELISA.

In our study we also considered the age of sampled camels, and of 60 sera samples, camels falling under the age of 9 years were more prone to the disease (28.33%), while on the other hand, camels aging more than 10 years (40 sera samples) were less prone (10%) to brucellosis. We think that camels that were less than 9 years lacking/or have lesser immunity, and this is not consistent with other studies, as this disease commonly persists in sexually mature camels (Radostitis et al., 1994; Walker, 1999).

We also collected the milk samples in order to detect the Brucella antibodies and the MRT was performed accordingly, for 50 milk samples. Interestingly, none of milk samples were found positive, which is not in agreement with the study of Al-Khalaf and El-Khaladi (1989), as they found 2 out of 3 milk samples positive by performing the same test.

Factors that contribute to the high prevalence rate of brucellosis in camels may be linked with the management system of camels in the studied districts. The mixing of camels during the time of migration, at watering time and/or in night enclosure can also play the transmission of the disease from infected animals to healthy ones.

Conclusion

The brucellosis is prevalent among the camels of study districts and the risk factors identified for individual animal seroprevalence included the sex and age. Hence, it is assumed that the disease likely spreads to unaffected camels and also the herds during the grazing and at watering points.

Acknowledgements

The study was ﬁnancially supported by the Ministry of Education, Youth and Sports of the Czech Republic- projects CENAKVA (No. CZ.1.05/2.1.00/01.0024), CENAKVA II (No. LO1205 under the NPU I program); by the Czech Science Foundation (No. P502/13/ 26952S) and COST Ofﬁce (Food and Agriculture COST Action FA1205: AQUAGAMETE).

Conflict of interest statement

We declare that we have no conflict of interest.

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