Human brucellosis caused by raw dairy products: A review on the occurrence, major risk factors and prevention

Highlights

• An up-to-date review on brucellosis occurrence and risk factors in dairy products is presented.

• Raw milk and cheeses produced from raw milk are the main vectors of human brucellosis.

• The main Brucella spp. responsible for human brucellosis are B. abortus and B. melitensis.

• Cattle, camel, goat or sheep raw milks are commonly contaminated with Brucella in endemic regions.

• Bacterial isolation and molecular approaches should be applied to detect and characterize foodborne Brucella infections.

Abstract

Despite considerable efforts made to address the issue of brucellosis worldwide, its prevalence in dairy products remains difficult to estimate and represents an important public health issue in many areas of the globe today. This is partly explained by the increasing tendency for consumption of raw dairy products, making the prevention and control of this zoonosis even more critical. This review summarizes reports published since the early 2000s on human brucellosis caused by contaminated dairy products and the systems of evaluation and assessment which are used to improve the diagnosis, surveillance, control and prevention of the disease. For this purpose, five comprehensive electronic databases were investigated and relevant studies were identified for systematic review. The design and quality of the studies revealed notable variation, especially in the methods used for the detection and characterization of Brucella spp. This report provides helpful information about the health risk associated with the consumption of raw milk and relevant preventive strategies.

Introduction

Brucellosis is a widespread zoonosis caused by closely related bacterial species belonging to the genus Brucella. This disease is mainly transmitted to humans through the consumption of contaminated dairy products (Kaynak-Onurdag et al., 2016; Oliver et al., 2009; Verraes et al., 2015). Brucellosis has been identified by the World Health Organization (WHO), the Office International des Epizootics (OIE) and the Food and Agriculture Organization of the United Nations (FAO) as one of the most significant neglected zoonotic diseases in the world (Corbel, 1997; Franc et al., 2018; Hosein et al., 2016; McLeod, 2011; Musallam et al., 2016). Brucellosis also generates significant economic impact by causing serious production losses through abortions, infertility, and decreased milk production in cattle, goats, sheep, swine and camels (McLeod, 2011).

Brucella melitensis represents the most virulent species for humans, although B. abortus, B. canis, B. suis (Corbel, 1997; Whatmore, 2009; Young, 1995) and, more rarely, the marine Brucella strains such as B. ceti and B. pinnipedialis (Dawson et al., 2008; McDonald et al., 2006) or B. inopinata (De et al., 2008; Scholz et al., 2010), can cause serious infections. Long term clinical signs of human brucellosis include sweats, arthralgia, undulant fever, back pain, hepatomegaly, abdominal pain, headaches, myalgia, and personality changes (Buzgan et al., 2010; Cutler et al., 2005; Valderas and Roop, 2006). Some other brucellosis symptoms are arthritis, leukopenia, anemia, hepatitis, thrombocytopenia, endocarditis, and meningitis (Buzgan et al., 2010). Brucellosis is most commonly associated with the consumption of contaminated dairy products, but has also been reported following close contact with infected animals and among microbiology laboratory workers (Corbel, 1997; Staszkiewicz et al., 1991). Although brucellosis has been eradicated in some developed countries, it still represents one of the most economically important diseases in Latin America, the Middle East, North and East Africa and South and Central Asia (McDermott and Arimi, 2002; Musallam et al., 2016; Oliveira et al., 2017). One of the main issues in brucellosis-endemic regions is possible under-diagnosis and the lack of availability of specific treatment regimens to cure complicated brucellosis in humans in order to achieve universal care and control in susceptible populations (Buzgan et al., 2010).

Thus, Brucella contamination of raw dairy products remains one of the main concerns for dairy product consumers in developing countries (McDermott and Arimi, 2002; Oliver et al., 2009), while most developed countries try to maintain brucellosis-free status in livestock (Falenski et al., 2011). Recently, the increasing tendency for consumption of raw dairy products, not only from cows, sheep, and goats, but also camels, llamas, donkeys, horses, buffaloes, reindeer, and yaks (Falenski et al., 2011) constitutes an additional risk of brucellosis transmission. As an effective preventive strategy in the absence of pasteurization facilities, thermal treatment such as boiling or heating milk to a minimum temperature of 80–85° for several minutes (Corbel, 2006) can be used to control brucellosis. At farm level, control strategies should be supported by national eradication programs and a preliminary serological screening using a simple, rapid and cost-effective method such as Rose Bengal Test (RBT) appeared to be effective (Mustafa and Nicoletti, 1995). In addition, vaccination campaigns for small ruminants and cattle have been used in some countries and could represent a cost effective and useful control approach for both health and agricultural sectors (Roth et al., 2003).

The purpose of the current review is to summarize current data about virulent Brucella spp. contaminating different dairy products and different methods/conditions used for their detection. The Brucella hazards reported in raw milk of different animal species such as cows, sheep, goats, and camels are also highlighted.