Review Article

 

Prevalence of Bovine and Human Brucellosis in Pakistan–A Review

 

Aamir Shehzad, Fedik Abdul Rantam*, Wiwiek Tyasningsih, Saifur Rehman

Microbiology Veterinary Division, Faculty of Veterinary Medicine, University of Airlangga, Surabaya, Indonesia.

 

Received | December 08, 2020; Accepted | December 19, 2020; Published | February 15, 2021

*Correspondence | Fedik Abdul Rantam, Microbiology Veterinary Division, Faculty of Veterinary Medicine, University of Airlangga, Surabaya, Indonesia; Email: fedik-a-r@fkh.unair.ac.id

Citation | Shehzad A, Rantam FA, Tyasningsih W, Rehman S (2021). Prevalence of bovine and human brucellosis in pakistan–a review. Adv. Anim. Vet. Sci. 9(4): 473-482.

DOI | http://dx.doi.org/10.17582/journal.aavs/2021/9.4.473.482

ISSN (Online) | 2307-8316; ISSN (Print) | 2309-3331

Copyright © 2021 Rantam et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

 

Introduction       

 

Brucellosis is one of the important and widespread zoonoses around the globe except in some counties of high income (Poester et al., 2002; Pappas et al., 2006; OIE, 2009). Brucellosis is the most neglected and unrecognized infection not only in the world but also in Pakistan (Rubach et al., 2013; WHO, 2012). The disease is caused by a gram-negative bacteria Brucella that has so far twelve identified species (Rajala, 2016). Mostly Brucella species can cause disease in multiple species of animals including humans (Godfroid et al., 2010). In bovines, Brucella abortus is predominantly responsible for Brucellosis, while less frequently caused by Brucella melitensis and occasionally by Brucella suis (OIE, 2016). It is an important infection of sexually matured animals that can cause significant reproductive losses, in-terms of last trimester abortion, infertility, stillbirth, orchitis, placentitis and also causes possible excretion of the organism in uterine discharges and milk (Forbes & Tessaro, 1996; Wadood et al., 2009; England et al., 2004; Corbel et al., 2006; Islam et al., 2013). Infected animals mostly abort once but remain infected throughout their entire life (Godfroid et al., 2010). Brucellosis is not only one of the most important diseases in prospective of animals and human health but also it has socio-economic importance in rural areas due to dependence on livestock and dairy products for income generation and livestock is considered as a lifeline for the 95% rural population of the developing countries (Maadi et al., 2011; Wadood et al., 2009; Hoffmann, 1999). Bovine Brucellosis is also a disease of yak, buffalo, and bison that causes similar signs and symptoms to those seen in cattle (OIE, 2009).

 

Worldwide, twelve Brucella species have been recognized but have two important members, Brucella melitensis and Brucella abortus that affect mainly sheep, goats, and bovines (cattle & buffalo) respectively. Furthermore, there are other ten species of Brucella including B. suis, B. canis, B. ovis, B.neotomae, B. microti, B. pinnipedialis, B. ceti, B. papionis, B.vulpis, B. inopinata (Corbel, 1998; Whatmore, 2009). Transmission of the disease occurs in the herd mostly due to the ingestion of bacteria from the aborted fetuses, placenta, and discharges of cattle that contaminate pauster or water. (Park et al., 2005).

 

Pakistan is a country with more than 207.8 million people with one of the world’s fourth-leading milk-producing countries that produce yearly 54,328 thousand tons of milk (Pasha & Hafiz, 2017; ESOP, 2014, Iqbal & Ashraf, 2017). Pakistan has the sixth-largest livestock-based economy in the world with an animal population of 186.2 million. Furthermore, about 30 million people or 8 million families have their earnings from the livestock sector and the majority of them live in rural areas of Pakistan. Livestock sector productions have a major contribution of approximately 60 % of agriculture and 11.2 % of Pakistan gross domestic product (GDP), (Jan & Akram, 2018; GoP, 2019; Chandio et al., 2017). 

 

In Pakistan, cattle and buffaloes have cultural, dietary, and economic impacts that accomplished their worth in our rural society but the spread of infectious diseases especially Brucellosis is an emerging hazard for the livestock of Pakistan. The main causes of Brucella spreading are improper surveillance, under-reporting, lack of knowledge, the informal markets of raw milk, and the absence of proper legislation about the Brucella prevalent animals. The current review, therefore, focuses on Pakistan, where bovine Brucellosis is common but still under-researched and reported. The objectives of the current review are to summarize the prevalence and zoonotic importance of Brucellosis in Pakistan. This study also provides relevant information and conceptual ideas that will help in controlling and eradication of Brucellosis in Pakistan.

 

Material and Methods

 

A comprehensive search was made to identify the relevant studies and data published from 2000 to May, 2020 by using major databases of Google Scholar, PubMed and Google search engine. The keywords used were Seroprevalence, bovine, human Brucellosis, risk factors, and suitable combinations of the above to make sure the search for relevant studies.

 

Inclusion and Exclusion Criteria

The basic criteria for the selection of articles was based on the following serological tests: Rose Bengal plate test (RBPT), milk ring test (MRT), serum agglutination test (SAT) and enzyme-linked immunosorbent assay (ELISA). The paper published from January 2000 to May 2020 that are available on Google scholar, PubMed and Google search engine were included in the current review study. The peer reviewed articles on human and bovine Brucellosis that were published in the English language were also considered in the current study. The articles published other than English language, Conference Papers and those without peer reviewed were excluded from the study.

 

Characteristics of the Study

Initially, a total number of 1250 titles of published articles were read and 146 articles were selected for the further consideration. After removing duplicates the abstracts of 119 articles were selected for screening. The abstracts of 72 papers after screening were excluded and the remaining 47 articles were selected for the full paper review. After full screening of the articles another 18 papers were excluded that did not match our inclusion criteria. The remaining 29 articles were included in the study for quality data analysis. In the selected articles three (3) studies were on cattle, buffaloes, and humans, ten (10) on buffaloes and cattle, while Seven (7) Five (5) and four(4) studies were conducted only on cattle buffaloes and human respectively as shown in Figure-1, Table-1.

 

Epidemiology and Seroprevalence of Bovine Brucellosis in Pakistan

Compact and precise sampling design is considered basic for any epidemiological study, in the current review, it is found that many studies have no proper criteria for animal selection and applied non-randomization techniques for their studies or surveys. The exact incidence of Brucellosis is still unknown in Pakistan but it varies due to the species’ sex, age, geographical and climate conditions. Moreover, its spread is mainly influenced by the husbandry system as well as environmental conditions (Gul and Khan, 2007; WHO, 1997).

 

Punjab is the second largest province in terms of land size area and the largest human and animal populated province of Pakistan (Ghori et al., 2017; PBTI). In the current review, a total of fourteen (14) studies were included in cattle and buffaloes of Punjab province and found an overall average frequency of Brucellosis of 8% and 7.26% in cattle and buffaloes respectively. (Table-1). In cattle, the seroprevalence based on 14 different studies were found between the range minimum of 2.05% to a maximum of 28.90% (Nawaz et al., 2016; Ullah et al., 2019) (Table 1). Two studies were conducted on cattle at the Pothohar region, northern salt range areas of province Punjab, and found 3.60% lower Brucellosis incidence through MRT but a similar type of study was performed in the same region and found 5.01% seroprevalence in cattle. (Ali et al., 2014; Shahzad et al., 2015). Studies of cattle at government farms, private farms and in different villages portray a huge Brucella incidence variation; a survey study was executed at properly managed government livestock dairy production research institute, Bahadar Nagar, district Okara and reported 14.11% Brucellosis in cattle (Chaudhry, 2000) but later on another study was conducted at all government livestock dairy farms which revealed a low incidence of 2.15% of Brucellosis in cattle (Jamil et al., 2020). At government livestock farms, better husbandry techniques were practised than that of private farms. In comparative surveillance conducted at private and government farms reported overall 15.40% prevalence in cattle while comparatively a higher frequency of Brucellosis is found at private than that of government livestock farms in cattle (Nasir et al., 2004). Hussain et al. (2008) described in their study the seroprevalence of cattle at different villages and livestock farms and reported a 10.18% seroprevalence of Brucellosis in cattle. 

 

A study on large scale in thirty-six districts of Punjab was performed in which 59665 serum samples were collected from the bovine and found a prevalence of 2.05% in cattle (Nawaz et al., 2016). Later on similar studies were conducted in northern Punjab Rawalpindi area by Ahmad et al. (2017) and southern belt district Rejanpur by Ismail et al. (2018) to determine the seroprevalence of Brucellosis in cattle and it was found 8.1% high prevalence rate in the northern areas Rawalpindi region as compared to 4.4% in cattle at Rajanpur. Meanwhile it was found a low prevalence of 3.8% in cattle in the eastern districts of Punjab Okara, Faisalabad, Kasur and Lahore (Saeed et al., 2019). A study was designed for the diagnosis of Brucella prevalence in cattle and buffaloes at desert Thal area of district Bhakkar and found a prevalence of 11.9% in cattle respectively (Shehzad et al., 2020).

 

In buffaloes frequency of brucellosis is based on 16 articles in which a high prevalence of 21.73 % was found in districts: Lahore, kushab, Bhakkar, khanewal, Gujranwala of Punjab province while a low prevalence of 1.6% was reported in northern Punjab district Rawalpindi and nearby areas of Islamabad (Nasir et al., 2004; Ahmad et al., 2017). Different studies on seroprevalence of Brucellosis in buffaloes revealed variation in results likewise at government livestock dairy production research institute, Bahadar Nagar, district Okara, at private livestock farms and in different villages, found 11.17%,21.73% and 9.38% respectively (Chaudhry, 2000; Nasir et al., 2004; Hussain et al., 2008). A comprehensive and large scale study was conducted in all 36 districts of Punjab and found an overall very low prevalence of 7.86% of Brucellosis in buffaloes as compared to all previous studies (Nawaz et al., 2016). In the northern Punjab Potohar area, the seroprevalence of Brucellosis in buffaloes was reported quite low at 1.6% as compared to 5.2% in south Punjab district Rajanpur (Ahmad et al., 2017; Ismail et al., 2018).

 

Balochistan is area wise the largest province of Pakistan in terms of land size but 4.9% of the human population lives there. Livestock is a very important source of food and income generation for the rural population of Balochistan province and the livestock population of Balochistan is 20% of the total national population of Pakistan. The buffaloes are at very low numbers of 300000 heads but have a good cattle population of 2.3 million (Kakar et al., 2008). There were conducted two studies on cattle Brucellosis by using blood serum in Baluchistan province and found a maximum prevalence of 3.95% in Quetta area while slightly low 3.5% in the district Lorelai (Shafee et al., 2012; Khan et al., 2016). Only one study was executed on buffaloes by using raw milk for the diagnosis of Brucella incidence at the Quetta area and reported 1.7% Brucellosis (Shafee et al., 2011).

 

Sindh is the third largest province of Pakistan. The livestock population is an important component of the agriculture sector (Wasim, 2007). A serological study was carried out for the determination of Brucellosis reported a 25% rate of Brucella infection in cattle but another report of Brucellosis incidence in buffaloes showed a very low infection of 1.99% (Mangi et al., 2015; Yousaf et al., 2016). 

 

Brucella infection causes abortion in both cattle and buffaloes and in a study executed at Hyderabad District of Sindh for the diagnosis of brucellosis in bovines having a history of abortion revealed a very high prevalence rate of Brucellosis of 31.88% and 47.19% in cattle and buffaloes respectively (Soomro et al., 2014). 

 

Khyber Pakhtunkhwa (KPK) is the third largest province of Pakistan in terms of livestock and human population. According to the Livestock Census (2006), it has buffaloes of about 808068 heads of lactating, 184229 dry and 97664 without calving and has cattle of about 6059041 heads lactating, 6059041 dry, and 6059041 without calving. Very high seropositivity of 17.58% was found in cattle at government Livestock District Kohat but a low prevalence of 3.97% was reported in two districts, Banu and Laki Marwat. (Hamidullah et al., 2009; Bakhtullah et al., 2014) while a study of Brucellosis in buffaloes revealed an 11% incidence in the Swat valley of KPK (Khana et al., 2017). 

 

Gilgit Baltistan (GB) is the fifth province of Pakistan with a very low bovine population. Only one study was executed for the determination of Brucella infection in cattle at Ghizer, Skardu and Gilgit districts of GB and found 10.93% Brucellosis (Saher et al., 2018) (Table-1).

 

In milk-based samples, MRT was used and reported a low prevalence of 1.7% in raw milk of buffaloe at Quetta while maximum prevalence was found 47.19% in Hyderabad province Sindh. Similarly in cattle prevalence of Brucellosis in raw milk reported 31.88% at Hyderabad while a low prevalence of 2.25% was found in Lorelai Balochistan (Soomro et al., 2014; Khan et al., 2016).

 

RBPT test was applied in 21 out of 29 studies and was additionally reconfirmed through SAT in 5 studies and by ELISA in 12 studies respectively. The maximum seroprevalence of Brucellosis confirmed with SAT and ELISA was 17.58% and 27.86% respectively while the lowest prevalence 1.75% and 1.2% were found in cattle respectively (Khan et al., 2016; Ismail et al., 2018; Hamidullah et al., 2009; Ullah et al., 2019). Similarly, the higher seroprevalence of 9.51% and 13% were found while the lower of 7.64% and 1.21% by SAT and ELISA were found respectively in buffaloes (Nasir et al., 2004; Khana et al., 2017; Chaudhry, 2000; Shehzad et al., 2020).

 

Effect of age on Brucellosis

Age is an important factor that affects the prevalence of Brucellosis. Chaudhry, (2000) reported that seroprevalence in adult cattle and buffalo of  2-10 years was found high as compared to the young age of under 2 years of cattle and buffalo. In a similar type of study, Nasir et al. (2014) recorded that Brucellosis is high in buffaloes of 3years old or more. While Saeed et al. (2019) determined that adult or mature cattle and buffaloes are more prevalent for Brucellosis than young ones. Whereas studies executed by Bakhtullah et al. (2014) and Mangi et al. (2015) showed cattle having an age group of more than four years is more prevalent for Brucellosis. Similarly in a recent study regarding seroprevalence of Brucellosis, it has been declared that in mature, pregnant, and lactating cows incidence of Brucella is quite higher than in immature, dry, and non-lactating ones (Khan et al., 2020).

 

Effect of sex on Brucellosis

Nasir et al. (2014) used RBPT and SAT for seroprevalence of Brucellosis in buffaloes and detected seroprevalence of Brucellosis quite higher in female buffaloes than in males, while another study conducted in Okara, Faisal Abad, Kasur, Lahore districts of Punjab, reported a difference in results to the previous ones that males were more prevalent than females (Saeed et al., 2019). Shafee et al. (2012); Mangi et al. (2015) diagnosed seroprevalence of Brucellosis in cattle and buffaloes and stated a quite higher rate of seroprevalence in female than male.

 

Effect of species on Brucellosis

Soomro et al. (2014); Nawaz et al. (2016); Saeed et al. (2019); Jamil et al. (2020) reported that Brucellosis seroprevalence is higher in buffaloes than in cattle while in a recent study by Shehzad et al. (2020) reported contrary that Brucellosis in cattle is higher than in buffaloes.

 

Effect of breeds on Brucellosis

Shahzad et al. (2015); Mangi et al. (2015); Bakhtullah et al. (2014); Khan et al. (2020) found in their studies that seroprevalence of Brucellosis is higher in exotic cattle and Friesian cross with local breeds than in local breeds of Pakistan, while Khan et al. (2016) reported differently with previous studies that Brucella is higher in the local breed in district Lorelai than crossbred cattle.

 

Effect of management systems on Brucellosis  

Nasir et al. (2004) investigated the seroprevalence of Brucellosis on government and private livestock forms and reported a higher prevalence rate in private livestock farms due to poor management as compared to in government livestock farms having proper management. On the contrary Shafee et al. (2011) reported higher prevalence at government dairy farms in Quetta than in private farms. According to the research of Bakhtullah et al. (2014), Brucellosis is more prevalent in free-grazing cattle in field areas as compared to stall feeders.

 

Table 1: Seroprevalence of Bovine and Human Brucellosis reported in different regions /areas of Pakistan

 

Province / Region	District/Area	Prevalence %				Source	Species
		RBPT	SAT	MRT	Elisa
Punjab	Okara	14.11	10.0	-	-	Chaudhry, (2000)	Cattle
	Lahore, kushab, Bhakkar, khanewal, Gujranwala.	15.40	7.50	-	-	Nasir et al., 2004
	Dairy Farms ,Villages of Punjab	10.18	-	-	8	Hussain et al., 2008
	Potohar plateau, Chakwal, Attok, Rawalpindi.	-	-	3.60	-	Ali et al., 2014
	Potohar region	5.01	-	-	-	Shahzad et al., 2015
	All 36 district of Punjab	2.05	-	-	-	Nawaz et al., 2016
	Rajanpur	4.4	-	-	1.2	Ismail et al., 2018
Capital/ Punjab	Islamabad, Rawalpindi	8.1	-	-	6.6	Ahmad et al., 2017
Punjab	Okara, Faisal abad,Kasur, Lahore	3.8	-	-	-	Saeed et al., 2019	Buffaloes
	L&DD Dairy Farms	2.15	-	-	1.91	Jamil et al., 2020
	Gujranwala Division	28.90	-	-	27.86	Ullah et al., 2019
	Faisalabad	12.53	-	-	2.40	Khanet et al., 2020
	Bhakkar	11.9	-	-	2.29	Shehzad et al., 2020
	District Okara	11.17	7.64	-	-	Chaudhry, (2000)
	Lahore, kushab, Bhakkar, khanewal, Gujranwala	21.73	9.51	-	-	Nasir et al., 2004
	Dairy Farms ,Villages of Punjab	9.38	-	-	6.92	Hussain et al., 2008
	Potohar plateau, Chakwal, Attok, Rawalpindi.	-	-	3.09	-	Ali et al,.2014
	Dera Chal other private farms	12.2	-	-	-	Nasir et al,.2014
	All 36 district of Punjab	7.86	-	-	-	Nawaz et al., 2016
	Rajanpur	5.2	-	-	2.0	Ismail et al., 2018
	Okara, Faisal abad,Kasur, Lahore	5.1	-	-	-	Saeed et al., 2019
	L&DD Dairy Farms	5.62	-	-	4.64	Jamil et al., 2020
	Bhakkar	7.2	-	-	1.21	Shehzad et al., 2020
Capital/ Punjab	Islamabad, Rawalpindi	1.6	-	-	1.6	Ahmad et al., 2017
Punjab	District Okara	15.71	11.43	-	-	Chaudhry, (2000)	Human
	Dairy Farms ,Villages of Punjab	14	-	-	11	Hussain et al., 2008
	Rawalpindi	5.8	-	-	-	Ali et al., 2016
	Rawalpindi	10.1	-	-	-	Saddique et al., 2019
	All Punjab	16%	-	-	-	Ali et al., 2018
	Bhakkar	17.74	-	-	-	Shehzad et al., 2020
	Lahore	-	-	-	21.7%	Mukhtar et al., 2008
Balochistan	Quetta	3.95	-	-	5.9	Shafee et al., 2012	Cattle
	Quetta	-	-	4.6	20	Shafee et al., 2011
	Loralai	3.5	1.75	2.25	-	Khan et al., 2016
	Quetta	2.1	-	-	2.6	Shafee et al., 2012	Buffaloes
		-	-	1.7	0	Shafee et al., 2011
KPK	KOHAT	17.58	17.58	-	-	Hamidullah et al., 2009	Cattle
	Banu & Laki Marwat	-	-	3.97	-	Bakhtullah et al.,2014
	Swat Valley	11	-	-	13	Khana et al., 2017	Buffaloes
Sindh	Haderabad	-	-	31.88	-	Soomro et al., 2014	Cattle
		25	23	2	11.8	Mangi et al., 2015
		-	-	47.19	-	Soomro et al., 2014	Buffaloes
		-	-	-	1.99	Yousaf et al., 2016
Gilgit Baltistan	Ghizer, Skardu and Gilgit	10.93	-	-	6.25	Saher et al., 2018	Cattle

 

Geographical and seasonal effects on distribution of Brucellosis

Nawaz et al. (2016) described a very higher Brucella prevalence in central districts of Punjab than in northern and southern Punjab while Saeed et al. (2019); Bakhtullah et al. (2014); recorded difference in seroprevalence of Brucellosis in different areas. Likewise areas, regions, and the seasons also affect the seroprevalence of Brucellosis as Yousaf et al. (2016) stated a higher rate of Brucellosis in winter than in summer season.

 

Associated risk factors of Brucellosis in bovines 

Ismail et al. (2018) recorded that bovines (buffalo & cattle) with abortion history showed a high rate of seroprevalence of Brucellosis. Furthermore it was found a positive correlation among Brucella positive animals and reproductive disorders like repeat breeding, metritis, and retention of fetal membrane. Saeed et al. (2019) and Shehzad et al. (2020) determined a high seroprevalence rate of Brucellosis in animals having a history of abortion. In another research executed by Ullah et al. (2019) reported a significant association between reproductive disorders (abortion, stillbirth, repeat breeders, and retention of the fetal membrane) and seropositive cattle of Brucellosis.

 

Isolation and identification of Brucella in bovines

Ali et al. (2014) collected samples of milk, vaginal swab, and aborted fetuses from the cattle and buffaloes and subjected them to the culturing procedures. For identification of Brucella strains, the researchers used the biotyping and molecular method and confirmed the B. abortus biovar 1 incidence in collected samples. Most of the studies reported incidence of Brucella abortus in seropositive buffaloes and cattle by using real-time (RT) PCR (Ahmad et al., 2017; Jamil et al., 2020). Meanwhile, in another study, the researchers reported Brucella melitensis in all seropositive samples of cattle and buffaloes by using RT-PCR (Saeed et al., 2019).

 

Human Brucellosis

The human frequency of Brucellosis was found in 7 out of 29 reviewed articles and all studies reveal occupational risks. There is no study that can explain the incidence of Brucellosis at the national level. The prevalence of Brucellosis was found 5.8% to 17.74% in different areas of the province Punjab, Pakistan (Ali et al., 2016; Shehzad et al., 2020). We have found no article used in the current study, that can reveal the human Brucellosis incidence in other provinces of Pakistan.

 

Hussain et al. (2008) carried out a study to investigate Brucellosis in persons in close contact with animals like villagers, livestock and slaughterhouse workers. In this study, the researchers recorded overall 14% Brucella prevalence in humans and also reported a high prevalence rate in males, village workers, and abattoir associated personnel. Another study reported that Brucellosis is more prevalent in females of rural areas than the in the females of the urban areas and also it was found that seropositive females have symptoms and history of intrauterine fetal death, abortion, and miscarriage (Ali et al., 2016). The frequency of Brucella infection was recorded at a high rate in males and females having their ages equal or more than forty (40) years with the history of animal contact (Saddique et al., 2019). In a similar type of research work by Ali et al. (2018) recorded that males are more seropositive than females and described a high rate of prevalence in the age group of 20-30 years and also displayed that people who were resident of rural areas, kept animals in their homes and were uneducated, had a high rate of prevalence. Moreover, the researchers also described some associated potential risk factors like milking, exposure to animals, and slaughtering.

 

A study was conducted for the diagnosis of Brucellosis in persons in contact with animals like slaughterhouse workers, animal keepers, loaders, veterinary professionals, meat sellers, cleaners, and drivers. In this study it was found overall 21.7% Brucellosis in them, while the important diagnosis of the study was that Brucellosis was found at high rate in animal keepers (37.5%), illiterate workers and persons having old age 50-60 years (Mukhtar et al., 2008). A recent study by Shehzad et al. (2020) described that Brucellosis not only caused a high rate of abortion in spouses of seropositive humans but also is a predisposing factor for many other diseases. In the study, the researchers found a high rate of Brucellosis in married personals and in those people who consumed the raw milk. RBPT was used as a primary diagnostic tool for human Brucellosis in 6 (85.71%) studies but only in one study the researcher applied ELISA as a confirmatory test (Table 1). 

 

Economic impacts of Brucellosis

There is found no article regarding the economic impacts of Brucellosis in Pakistan. 

 

Discussion

 

The current review aimed to portray the trends of Brucellosis infection in cattle, buffaloes, and humans and explore the association between seropositivity and potential risks of Brucellosis in Pakistan. The reviewed serological data for the current study reveals strong evidence of Brucellosis spread in Pakistan not only in cattle and buffaloes but also in humans especially those remaining in close contact with animals. However, we found only 29 studies that are considered to have quality data useful for the estimation of the Brucella burden in Pakistan. The quantity and quality of research about the epidemiology of Brucellosis are very limited. There is no description found about future incidence estimation and economic losses of disease in published literature. Additionally in the current review found a very limited validity and scope of studies that create hindrance for obtaining a true seroprevalence of Brucellosis. Most of the articles about the prevalence have very limited and unclear diagnostic designs and also found nonrandomized sampling approaches or small sample size which depicts limited inauthentic seroprevalence. There is also found in some articles a lack of standardized techniques for the diagnosis of Brucellosis which leads to a misleading estimation of prevalence. For proper estimation and understanding of Brucellosis epidemiology, it is considered that the isolation of species and characterization of the prevalent biovars of Brucella are very essential, because all serological tests used for incidence are useful but have limited specification and sensitivity.

 

Seven studies revealed the incidence of Brucellosis in humans but there is no study that describes the isolation of Brucella species. So the accurate data about prevalence of Brucella species in humans is very necessary for the future control and eradication programs for Brucellosis.

 

In animals, the majority of studies about Brucellosis incidence is carried out with serological tests i.e. RBPT, SAT, MRT based and in RBPT and MRT, locally prepared antigens are used for diagnosis. But only 8 out of 18 studies described the manufacturers of antigens. ELISA has been used as a confirmatory test in 13 studies and has been proved more sensitive, accurate and specific. No researcher described any Brucella vaccination history in his research about the diagnosis of Brucellosis through serological tests. This review found the highest seroprevalence of 25% and the minimum of 2.05% in cattle through the blood serum samples and similarly found a high rate of 21.73% and minimum of 1.6% in buffaloes (Mangi et al., 2015; Nawaz et al., 2016; Ahmad et al., 2017; Nasir et al., 2004).

 

The seroprevalence of Brucellosis in bovine varied due to geographical and environmental conditions, different breeds, sexes, and the difference in ages as within cattle varied from 2.05% to 28.90%, 7.50% to 11.43%, 3.09% to 43.19%, and 1.91 to 27.86 through the serological tests RBPT, SAT, MRT, and ELISA respectively. Moreover, the prevalence was found in buffaloes 1.6% to 21.73%, 7.64% to 9.51%, 3.09 to 47.19%, and 1.21% to 6.92 through the serological tests RBPT, SAT, MRT, and ELISA respectively (Nawaz et al., 2016; Ullah et al., 2019; Nasir et al., 2004; Chaudhry, (2000); Ali et al., 2014; Jamil et al., 2020; Ahmad et al., 2017; Soomro et al., 2014; Shehzad et al., 2020; Hussain et al., 2008). There is found a huge variation in the results of Brucella prevalence. It may be due to geographical distribution, the difference in husbandry techniques and might be due to seasonal or environmental effects as some articles reported that the rate of prevalence varied area to area and also change under different environmental conditions (Nawaz et al., 2016; Bakhtullah et al., 2014; Yousaf et al., 2016). Similarly in the same region or area, a difference in the incidence of Brucellosis is found. Two studies conducted in pothohar, found variations in Brucella incidence in cattle; it might be due to the difference in applied diagnostic techniques (Ali et al., 2014; Shahzad et al., 2015).

 

Association between reproductive disorders and seropositivity of Brucellosis in bovines found in 4 out of 29 studies and also especially found a significant relationship among the abortion and seropositive animals (Ismail et al., 2018; Saeed et al., 2019; Shehzad et al., 2020; Ullah et al., 2019; Saddique et al., 2019; Mukhtar et al., 2008). 

 

None of the studies out of the 29 reviewed articles revealed the incidence of Brucella species or biovars in humans and also can explain species based association between animal and human Brucellosis. Most of the studies were conducted about the incidence of Brucellosis in humans who are in close contact with animals or veterinary professionals (Hussain et al., 2008; Ali et al., 2016). But only one study found about the use of unpasteurized milk in seropositive humans and also threw light on the risks associated with human to human and reported miscarriages in the spouse of male seropositive for Brucellosis (Shehzad et al., 2020). There is a lack of a wide range and randomized seroprevalence study of Brucellosis in humans which can explain the true frequency of Brucellosis in humans in Pakistan.

 

Prevention, control, and eradication of Brucellosis in humans depend on the successful control strategy of diseased animals. The eradication goal has been achieved by some developed countries through the following steps: regular vaccination policy, continuous surveillance, slaughtering, or culling of positive animals, and strict control on the movement of animals from the pandemic area.  

 

Conclusion

 

In the current review of literature, it is summarized that bovine and human Brucellosis is highly prevalent in Pakistan but there is a need of a large scale systematic and randomized study program and approaches for the accurate and actual prevalence of Brucellosis. Moreover, studies are needed that can estimate the actual economic losses. The veterinary and public health authorities need to collaborate their efforts to develop a comprehensive and compact control program and implement it to minimize financial losses due to Brucellosis. It is found that there is no proper vaccination and culling program or stamping of seropositive animals. Therefore in the context of Pakistan, there is a need of the strengthening the surveillance and disease reporting systems and enhancing the diagnostic capabilities of laboratories in all districts. Awareness campaigns should be launched for the education of farmers regarding the hazards of Brucellosis.

 

Author’s contribution

 

The submitting author is responsible for ensuring that contributions of all authors are correct as authors, Aamir Shehzad, Wiwiek Tyasningsih and Saif ur Rehman have made their contributions in data search, selection and analysis of the quality of data, designing and drafting of the manuscript while the author Fedik Abdul Rantam critically reviewed the current study.

 

References

 

• Ahmad T, Khan I, Razzaq S, Akhtar R (2017). Prevalence of bovine brucellosis in Islamabad and rawalpindi districts of Pakistan. Pak. J. Zool. 49:1123-1126. https://doi.org/10.17582/journal.pjz/2017.49.3.sc5

• Ali S, Akhter S, Neubauer H, Scherag A, Kesselmeier M, Melzer F, Ali Q (2016). Brucellosis in pregnant women from Pakistan: an observational study. BMC. Infect. Dis. 16: 468. https://doi.org/10.1186/s12879-016-1799-1

• Ali S, Ali Q, Melzer F, Khan I, Akhter S, Neubauer H, Jamal SM (2014). Isolation and identification of bovine Brucella isolates from Pakistan by biochemical tests and Pcr. Trop. Anim. Health. Pro. 46:73-78.

• Ali S, Nawaz Z, Akhtar A, Aslam R, Zahoor MA, Ashraf M (2018). Epidemiological investigation of human brucellosis in Pakistan. Jundishapur. J. Microbiol. 11:7. https://doi.org/10.1007/s11250-013-0448-6

• Bakhtullah FP, Shahid M, Basit A, Khan MA, Gul S, Wazir I, Raqeebullah KR (2014). Sero–prevalence of brucellosis in cattle in southern area of Khyber Pakhtunkhwa, Pakistan. Res. J.Vet. Pract. 2: 63-66. https://doi.org/10.14737/journal.rjvp/2014/2.4.63.66

• Chandio AA, Rehman A, Jiang Y, Noonari S (2017). Importance of the dairy industry and economic growth in Pakistan: an empirical study. J. Appl. Environ. Biol. Sci. 7:13-20.

• Chaudhry MA (2000). Serological survey of brucellosis in man and various age groups of cattle and buffalo.

• Corbel MJ (1998). Brucella. J. Syst. Bacteriol. 2:842-844.

• Corbel MJ (2006). Food and Agriculture Organization of the United Nations, World Health Organization & World Organisation for Animal Health, 2006. Brucellosis in humans and animals. World Health Organization. https://apps.who.int/iris/handle/10665/43597

• Economic Survey of Pakistan (ESOP) (2014). Government of Pakistan.

• England T, Kelly L, Jones RD, MacMillan A, Wooldridge M (2004). A simulation model of brucellosis spread in British cattle under several testing regimes. Prev. Vet. Med. 63:63-73. https://doi.org/10.1016/j.prevetmed.2004.01.009

• Forbes LB, Tessaro SV (1996). Infection of cattle with Brucella abortus biovar 1 isolated from a bison in Wood Buffalo National Park. Can. Vet. J. 37:415.

• Ghori MT, Khan MS, Khan JA, Rabbani M, Shabbir MZ, Chaudhry HR, Ali MA, Muhammad J, Elschner MC, Jayarao BM (2017). Seroprevalence and risk factors of glanders in working equines–Findings of a cross-sectional study in Punjab province of Pakistan. Acta. Trop. 176: 134-139. https://doi.org/10.1016/j.actatropica.2017.07.031

• Ghori MT, Khan MS, Khan JA, Rabbani M, Shabbir MZ, Chaudhry HR, Ali MA, Muhammad J, Elschner MC, Jayarao BM. (2017). Seroprevalence and risk factors of glanders in working equines–Findings of a cross-sectional study in Punjab province of Pakistan. Acta. Trop. 176: 134-139. https://doi.10.1016/j.actatropica.2017.07.031. Epub 2017 Jul 29. PMID: 28760480.

• Godfroid J, Nielsen K, Saegerman C (2010). Diagnosis of brucellosis in livestock and wildlife. C.M.J. 51:296-305. https://doi.org/10.3325/cmj.2010.51.296

• GoP (2019). “Pakistan economic survey 2018-19”, Ministry of Finance and Economic Affairs, Government of Pakistan, Islamabad. June 2019.

• Gul ST, Khan A (2007). Epidemiology and epizootology of brucellosis: A review. Pak. Vet. J. 27:145-151.

• Hamidullah M, Khan R, Khan I (2009). Seroprevalence of brucellosis in animals in district Kohat NWFP and comparison of two serological tests. Pak. J. Med. Sci. 61: 242-243.

• Hoffmann D (1999). Asian livestock to the year 2000 and beyond. RAP Publication 25:1-44.

• Hussain I, Arshad MI, Mahmood MS, Akhtar M (2008). Seroprevalence of brucellosis in human, cattle, and buffalo populations in Pakistan. Turk. J. Vet. Anim. Sci. 32: 315-318.

• Iqbal MN, Ashraf A (2017). Buffalos in Pakistan: incidence and control of gastrointestinal parasitic infections in naturally infected water buffaloes. PSM. Vet. Res. 2: 33-34.

• Islam MRU, Gupta MP, Filia G, Sidhu P K, Shafi T A, Bhat S A & Mustafa R (2013). Sero–epidemiology of brucellosis in organized cattle and buffaloes in Punjab (India). Adv. Anim. Vet. Sci. 1: 5 – 8.

• Ismail M, Ahmad I, Khan MS, Ullah S, Malik MI, Muhammad K, Jan AA (2018). 19 Seroprevalance of Brucella abortus in cattle and buffaloes in district Rajanpur, Punjab, Pakistan. P.A.B. 7:556-564. https://doi.org/10.19045/bspab.2018.70069

• Jamil T, Melzer F, Saqib M, Shahzad A, Khan K K, Hammad HM, Neubauer H (2020). Serological and Molecular Detection of Bovine Brucellosis at Institutional Livestock Farms in Punjab, Pakistan. Int. J. Env. Res. Pub. He 17:1412. https://doi.org/10.3390/ijerph17041412

• Jan I, Akram (2018). Willingness of rural communities to adopt biogas systems in Pakistan: Critical factors and policy implications. Renew. Sust. Energ. Rev. 81:3178-3185. https://doi.org/10.1016/j.rser.2017.03.141

• Kakar M A, Raziq A, ul Haq K M, Faqir M (2008). Trends and potential in dairy production of Balochistan province. Pak. J. Agn. Sc. 45:259-262.

• Khan TI, Ehtisham-ul-Haque S, Waheed U, Khan I, Younus M, Ali S (2018). Milk Indirect-ELISA and Milk Ring Test for Screening of Brucellosis in Buffaloes, Goats and Bulk Tank Milk Samples Collected from Two Districts of Punjab, Pakistan. Pak. Vet. J. 38:105-108. https://doi.org/10.29261/pakvetj/2018.021

• Khan M, Abro SH, Abro R Rind, ul Haq M, Goraya MU, Maqbool K (2016). Occurrences of brucella abortus in serum and milk samples of cattle in loralai, balochistan (a cae study). Sci. Int. 28:1183-1186.

• Khan UD, Khan A, Gul ST, Saleemi MK, Du XX (2020). seroprevalence of brucellosis in cattle (bos taurus) kept in peri urban areas of Pakistan. Agrobiol. Records. 1: 6-10. https://doi.org/10.47278/journal.abr/2020.003

• Khana SI, Muti-ur-Rehmana SM, Khanc A, Shakeel M, Shah MA, Naseer (2017). Patho-Epidemiology of Bovine Brucellosis in Aza-kheli Buffalo in Pakistan. Veterinaria. 4:21-26.

• Livestock Census (2006).http://www.pbs.gov.pk/sites/default/files/aco/publications/pakistan-livestock cencus2006/pak-11a.pdf.

• Maadi H, Moharamnejad M, Haghi M (2011). Prevalence of brucellosis in cattle in Urmia, Iran. Pak. Vet. J. 31: 81-82.

• Mangi MH, Kamboh AA, Rind R, Dewani P, Nizamani ZA, Mangi AR, Vistro WA (2015). Seropre valence of brucellosis in Holstein-Friesian and indigenous cattle breeds of Sindh Province. Pak. J. Anim. He. Prod. 3:82-87. https://doi.org/10.14737/journal.jahp/2015/3.4.82.87

• Mukhtar F, Kokab F (2008). Brucella serology in abattoir workers,. J. Ayub. Med. Coll. Abbottabad. 20:57–61

• Nasir AA, Parveen Z, Shah MA, Rashid M (2004). Seroprevalence of brucellosis in animals at government and private livestock farms in Punjab. Pak. Vet. J. 24: 144-146.

• Nasir A, Ashraf M, Shakoor A, Adil M, Abbas T, Kashif M, Reichel M (2014). Co-infection of water buffaloes in Punjab, Pakistan, with Neospora caninum and Brucella abortus. Turk. J. Vet. Ani. Sci. 38:572-576. https://doi.org/10.3906/vet-1310-36

• Nawaz G, Malik MN, Mushtaq MH, Ahmad FM, Shah A A, Iqbal F, Khan A (2016). Surveillance of brucellosis in livestock in rural communities of Punjab, Pakistan. Pak. J. Agric. Sci. 29:392-398.

• OIE (2016). Infection with Brucella abortus, Brucella melitensis and Brucella suis. Rome: OIE (World Organisation for Animal Health OIE.

• OIE (2009). Brucellosis, O. B, Manual of diagnostic tests and vaccines for terrestrial animals. World Organisation for Animal Health OIE, Paris, 12-30.

• Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV (2006). The new global map of human brucellosis. Lancet. Infect. Dis.6: 91-99. https://doi.org/10.1016/S1473-3099(06)70382-6

• Park MY, Lee CS, Choi YS, Park SJ, Lee JS, Lee HB (2005) A sporadic outbreak of human brucellosis in Korea. J. Korean Med. 20: 941-946. https://doi.org/10.3346/jkms.2005.20.6.941

• Pasha D, Hafiz A (2017). Population Census 2017.

• Poester FP, Goncalves VSP, Lage AP (2002). Brucellosis in Brazil. Vet. Microbiol. 90: 55-62. https://doi.org/10.1016/S0378-1135(02)00245-6

• Punjab Board of Investment and Trade (PBIT) (2017).www.pbit.gop.pk/livestock

• Rajala E (2016). Brucella in Tajikistan-Zoonotic risks of urbanized livestock in a low-income country. SLU. 39-40.

• Rubach MP, Halliday JE, Cleaveland S, Crump JA (2013). Brucellosis in low-income and middle-income countries. Curr. Opin. Infect. Dis. 26:404-412. https://doi.org/10.1097/QCO.0b013e3283638104

• Saddique A, Ali S, Akhter S, Khan I, Neubauer H, Melzer F, El-Adawy H (2019). Acute febrile illness caused by Brucella abortus infection in humans in Pakistan. Int. J. Environ. Res. Public Health. 16: 1-10. https://doi.org/10.3390/ijerph16214071

• Saeed U, Ali S, Khan TM, El-Adawy H, Melzer F, Khan A U, Neubauer H (2019). Seroepidemiology and the molecular detection of animal brucellosis in Punjab, Pakistan. Microorganisms. 7: 1-12. https://doi.org/10.3390/microorganisms7100449

• Saher MM, Mushtaq MH, Ubaid-ur-Rehman Z, Ubaid-ur-Rehman Z,Shabbir MZ (2018). The seroprevalence of Brucella abortus in Yak, Zo and cows in three districts of Gilgit-Baltitan, Province. W J A S. 10:1658-1668.

• Shafee M, Rabbani M, Ahmad MUD, Ahmad MUD, Muhammad K, Sheikh AA, Awan MA, Shabbir MZ (2012). Seroprevalence of bovine brucellosis using indirect ELISA in Quetta Balochistan, Pakistan. J.A.P.S. 22: 125-127.

• Shafee M, Rabbani M, Sheikh AA, Razzaq A (2011). Prevalence of bovine brucellosis in organized dairy farms, using milk ELISA, in Quetta City, Balochistan, Pakistan. Vet. Med. Int. 2011:1-3. https://doi.org/10.4061/2011/358950

• Shahzad A, Heinrich N, Falk M, Iahtasham K, Muhammad I, Shamim A (2015). Brucellosis infection in local and exotic cattle of Punjab, Pakistan. In 2nd ICSAE 2015, International Conference on Sustainable Agriculture and Environment, September 30-October 03, 2015, Konya, Turkey. Proceedings book, volume I & II :329-332.

• Shehzad A, Rantam FA, Masud A, Ahmed S (2020). Seroprevalence and potential risk factors associated with brucellosis in the Desert Thal of Pakistan. H.V.M Bioflux. 12:47-52.

• Soomro AH, Kamboh AA, Rind R, Dawani P, Sarwar M, Abro SH, Awais MM (2014). A study on prevalence and risk factors of brucellosis in cattle and buffaloes in district Hyderabad, Pak. J. Anim. Health Prod. 2:33 – 37. https://doi.org/10.14737/journal.jahp/2014/2.3.33.37

• Ullah Q, Jamil H, Lodhi LA, Qureshi ZI, Ullah S, Jamil T, Zubair M (2019). Brucellosis is Significantly Associated with Reproductive Disorders in Dairy Cattle of Punjab, Pakistan. Pak. J. Zool. 51:1995-1997. https://doi.org/10.17582/journal.pjz/2019.51.5.sc10

• Wadood F, Ahmad M, Khan A, Gul ST, Rehman N (2009). Seroprevalence of brucellosis in horses in and around Faisalabad. Pak. Vet. J. 29: 196-198.

• Wasim MP (2007). Trends and growth in livestock population in Sindh: A comparison of different censuses. Indus. J. Manag. Soc. Sci. 1: 58-75.

• Whatmore AM (2009). Current understanding of the genetic diversity of Brucella, an expanding genus of zoonotic pathogens. Infect. Genet. Evol. 9: 1168-1184. https://doi.org/10.1016/j.meegid.2009.07.001

• WHO (1997). Emerging and other communicable disease surveillance and control. The development of new/improved brucellosis vaccines. Reports of the WHO Meet-ings, Geneva. 1–37.

• World Health Organization (WHO) (2012). Neglected zoonotic diseases (NZD). In: http://www.who.int/neglected_diseases/zoonoses/en/, Accessed 26 November, 2012.

• Yousaf A, Laghari R A, Shoaib M, Ahmad A, Malhi KK, Mughal GA, Khetran IB (2016). The prevalence of brucellosis in Kundhi buffaloes in District Hyderabad. Pakistan. J. Anim. Health Prod. 4: 6-8. https://doi.org/10.14737/journal.jahp/2016/4.1.6.8