Food-borne microorganisms are major pathogens affecting food safety and cause human illness worldwide as a result of consumption of foodstuff, mainly animal products contaminated with vegetative pathogens or their toxins. Most of these microbes have zoonotic importance resulting in significant impact on both public health and economic sectors. Bacteria are the causative agents of two-thirds of human food-borne diseases worldwide with high burden in developing countries. Hence, the objectives of this review paper are to highlight the background of food-borne bacterial pathogens and to review common major food-borne zoonotic bacterial pathogens. Food animals are the major reservoirs of many food-borne zoonotic bacterial pathogens, and food products of animal origin are the main vehicles of transmission. Meat, dairy products, and eggs are the main ways by which people are exposed to zoonotic bacteria. S. aureus, Salmonella species, Campylobacter species, L. monocytogenes, and E. coli are the major zoonotic bacterial pathogens which are the causative agents of food-borne illness and death in the world associated with consumption of contaminated animal products. Production of toxins and structural virulent factors are responsible for the pathogenesis of these bacteria. These major zoonotic bacteria cause human infections which are characterized mainly by gastrointestinal symptoms including nausea, vomiting, diarrhea, abdominal cramps, and other agent-specific symptoms. Some bacteria may cause severe complications. Conventional (culturing), serological, and molecular techniques are important for detection of these common zoonotic bacteria and their toxins in food. Good hygiene, GMP, sanitation in operating procedures, and implementation of standardized HACCP and pasteurization procedures are effective methods for the control and prevention. Currently, the emergence of multidrug-resistant zoonotic bacteria associated with consumption of contaminated animal products is a great concern for the public health, and there should be coordinated surveillance and monitoring system for food-borne zoonotic bacterial pathogens particularly in developing countries including Ethiopia.
1. Introduction
Ethiopia is believed to have the largest livestock population in Africa, with an estimated population of 60,392,019 cattle, 31,302,257 sheep, 32,738,385 goats, 2,007,829 horses, 461,665 mules, 8,845,589 donkeys, 1,418,457 camels, 56,056,778 poultry, and 6,523,969 beehives [1]. The livestock sector contributes about 45% to the agricultural gross domestic product (GDP), 18.7% to the national GDP, and 16–19% to the total foreign exchange earnings of the country. It is the source of industrial raw materials (milk, meat, and hides and skin) and high-value protein to potential consumers in Ethiopia [2].
The consumption of animal products like meat, milk, and egg is increased due to rapid human population growth, urbanization, per capita income raise, globalization, and the changes on consumer habits (preference of high-protein diet). This situation results in a high demand of food of animal origin and leads to intensive animal production and processing of products, especially mass production and movement of products globally. During this time, there may be defective processing practices at any point of the farm to fork chain which increase the chances of contamination and spread of food-borne pathogens [3, 4].
Food products may become contaminated at different stages along the food chain [5], could be during production, processing, distribution, preparation, and/or final consumption. The risk of food getting contaminated depends largely on the health status of the food handlers, their personal hygiene, knowledge, and practice of food hygiene [6].
According to World Health Organization (WHO), food-borne diseases are defined as diseases of infectious or toxic nature which are caused by the consumption of food or water [7]. Intoxication (toxin produced by the pathogens causes food poisoning), infection (ingestion of food containing pathogens), and toxicoinfections (producing toxins while growing in the human intestines) are the three types of food-borne diseases [3, 8].
Diseases of animal origin can be transmitted between humans and animals through direct contact, indirect environmental contact, and/or through food consumption [9]. Around 60% of human diseases are originated from animals, and approximately 75% of new emerging human infectious diseases are transmitted from vertebrate animals to humans [10].
Food-borne pathogens are microorganisms (i.e., bacteria, viruses, and fungi) as well as a number of parasites [11], and they are the primary cause of food spoilage and food-borne diseases [5]. Food-borne microbes are major problems affecting food safety and cause human infections after consumption of the animal products contaminated with microorganisms or their toxins [4].
Most of the pathogens have a zoonotic origin, and food products of animal origin are considered as major vehicles of food-borne infections [12]. Food-producing animals (cattle, chickens, pigs, turkeys, etc.) are the major reservoirs for many food-borne pathogens [4]. Animal products (meat, milk, egg, fish, etc.) and their products have high risk due to pathogen contents, natural toxins, adulterants, and other possible contaminants [13], and the risk of food-borne diseases in humans is increasing when consumption of food of animal origin is increased [14].
In recent years, food-borne pathogens become an important public health problem worldwide, and their impact on health (significant morbidity and mortality rate) and economy is increasingly recognized [5, 11, 15–17]. According to different reports, a huge number of people suffer from food-borne diseases each year worldwide [12], and around 600 million (10 people in the world) become ill due to the consumption of contaminated food [18]. Due to unrecognized or unreported outbreaks, statistical data of food-borne diseases are increased [5].
Food-borne diseases are major health problems both in developed and developing countries [19], but developing countries tend to suffer from the largest share of the burden of food-borne diseases [16]. According to the WHO, 30% of the population suffer from food-borne diseases each year in developed countries, and up to 2 million deaths are estimated per year in developing countries [19].
Nowadays, the awareness has been growing on the public health impact of zoonotic food-borne pathogens transmitted from animal-originated food [20]. There is emergence of new pathogens, and the way of transmission of known food-borne pathogens is changing or is now associated with new food vehicles [15]. The prevalence of multidrug-resistant (MDR) food-borne pathogens is increased after consumption of contaminated food due to the use of drugs for human therapy and animal farming which are responsible for more serious disease than susceptible bacteria [5, 21]. Drug resistance among the pathogens in common and food-borne pathogens in particular is an emerging problem [15, 22].
Prevailing poor food handling and sanitation practices, inadequate food safety laws, weak regulatory systems, lack of financial resources to invest in safer equipment, and lack of education for food handlers are the reasons for common occurrence of food-borne diseases in developing countries including Ethiopia [13, 16, 23, 24]. The habit of raw beef consumption [25], overcrowding, poverty, inadequate sanitary conditions, and poor general hygiene are also the factors of food-borne diseases in Ethiopia [26].
The public health importance of several bacterial pathogens associated with food of animal origin has been shown by studies conducted in different parts of the country [13]. However, there is a lack of reliable statistics on food-borne diseases as well as well-organized and documented information on the occurrence of such diseases due to poor or nonexistent reporting systems in Ethiopia as well as in most developing countries.
Therefore, the objectives of this review paper are as follows: To highlight about the background information of food-borne bacterial pathogens To review common major food-borne zoonotic bacterial pathogens
2. Food-Borne Zoonotic Bacterial Pathogens
2.1. General Background
Food-borne diseases occur as a result of consumption of contaminated food stuffs especially from animal products [26–29]. Food poisoning syndrome results from ingestion of a wide variety of food contaminated with pathogenic organisms (bacteria, viruses, parasites, and fungi) and their toxin and chemicals. Bacteria (66%), chemicals (26%), virus (4%), and parasites (4%) are the main causes of food-borne diseases [8]. Currently, food-borne disease caused by bacterial contamination is one of the biggest issues affecting human health and food safety [30].
Bacteria are the causative agent of two-thirds of food-borne disease outbreaks though there have been around 250 different food-borne diseases [31]. From the biological hazards, bacterial pathogens are the most serious concern regarding the issues of meat safety to consumers [32]. Bacterial food-borne illnesses are among the most widely spread global public health problems in recent times [8].
Vertebrate animal species are natural reservoirs for many pathogens that cause human infections after transmitted through food [33]. Food of animal origin particularly meat (beef, mutton, and pork), dairy products (milk, cheese, yoghurt, and ice cream), and eggs are the three ways by which people are exposed to pathogenic bacteria [19]. Due to their nutritional value, mainly high protein and lipid content, dairy products are a suitable growth environment for a range of microorganisms [34]. Contaminated raw meat is one of the main sources of food-borne disease [26].
Food of animal origin (milk, meat, and their products) can become contaminated with bacteria during food processing or slaughtering [35]. These pathogens come into contact with food during harvest or slaughtering, processing, storage, and packaging. Environmental challenges have caused food-borne bacterial pathogens to evolve and the susceptibility of the human population to infections [5]. The battle against bacterial food-borne diseases is facing new challenges due to rapidly changing patterns of human consumption, the globalization of the food market, and climate change [31].
Food-borne bacterial diseases caused by bacteria are most commonly prevented and controlled by proper cooking and preparing of food as well as storing. The control method or measures also include education of those who prepare the food at home and other food handlers, prohibiting individuals with abscess or other skin lesions from handling food, and placing of food in a cold place at 4°C or lower temperature which prevent bacterial multiplication and toxin formation. Food must be kept at room temperature for as little time as possible [8].
2.2. Common Major Food-Borne Zoonotic Bacterial Pathogens
Among the bacteria that cause food-borne poisoning, some are particularly important in terms of frequency and/or of seriousness of the disease. Miscellaneous bacteria (including Gram positive and Gram negative) produce toxins that cause food-borne poisoning, resulting symptoms ranging from gastrointestinal disorders to paralysis and death [36]. It has been reported that Gram-negative bacteria account for approximately 69% of the cases of bacterial food-borne disease [24].
Although there are 31 pathogens that have been identified as causing food-borne diseases [11], bacterial pathogens including Staphylococcus aureus (S. aureus), Salmonella species, Campylobacter species, Listeria monocytogenes (L. monocytogenes), and Escherichia coli (E. coli) are the common causes of food-borne diseases and death in the world [5, 11, 20, 27, 37].
2.2.1. Staphylococcus aureus
The name Staphylococcus (staphyle = bunch of grapes in Greece) was introduced in 1883 by Ogston [31]. S. aureus is one of the most common food-borne pathogens worldwide [21, 38] with high occurrence second to salmonellosis [39].
It is a microorganism that is present as a commensal on the skin, nose, and mucous membranes of healthy humans and animals [39, 40]. However, it is a well-known opportunistic food-borne pathogen [41, 42] that can cause multiple infectious diseases of diverse severity [40]. It causes wide spectrum of diseases in both humans and animals [43].
The presence of S. aureus in products for human consumption is important to the food industry, as some strains are the cause of food-borne intoxication [21]. They are responsible for food spoilage, reduction of food safety, and shelf life and cause food-borne poisoning [44]. S. aureus is a leading cause of food poisoning resulting from the consumption of contaminated food with staphylococcal enterotoxins [45].
It earns public attention due to increasing mortality associated with multidrug resistance [21]. The widespread use of antibiotics and ability of the bacteria to rapidly develop and acquire antimicrobial resistance have facilitated the emergence of resistant strains such as methicillin-resistant S. aureus (MRSA) [41, 42, 46]. The emergence of MRSA in livestock and the possibility of human cross-contamination have caused a serious concern [38].
MRSA were first reported in the early 1960s and are now regarded as a major hospital-acquired pathogen worldwide [47]. MRSA is a well-known pathogen occurring both in human and veterinary medicine [21, 48].
(1) Etiology. The genus Staphylococcus comprises several species and subspecies [44]. S. aureus is a Gram-positive, catalase-positive, coagulase-positive, usually oxidase-negative, and facultative anaerobic coccus, which belongs to the family of Micrococcaceae [43, 49]. It is a nonmotile bacterium. Cells are spherical single and often form grape-like clusters [31]. Gold colony pigmentation, production of coagulase, fermentation of mannitol and trehalose, and production of heat stable thermonuclease distinguish S. aureus from other staphylococcal species [49]. The organisms are able to grow in a wide range of temperatures (7°C to 48°C with an optimum of 30°C to 37°C), pH (4.2 to 9.3, with an optimum of 7.0 to 7.5), and sodium chloride concentrations (up to 15% NaCl). These characteristics enable the bacteria to survive in a wide variety of food, especially those that require manipulation during processing, including fermented food products like cheese [31].
(2) Epidemiology. The epidemiology of this microorganism in animals has gained interest because of its importance in veterinary medicine, the increment of infectious processes caused by this pathogen (especially MRSA strains), and the emergence of some clonal lineages associated with animals, and zoonotic potential evidence is increased in the last years [40]. S. aureus is among the leading causes of food-borne bacterial intoxications worldwide [50]. It is one of the most common causes of reported food-borne diseases in the United States [7].
Around 50% of healthy individuals harbor the bacteria in their nasal passage, throat, and skin, whereas the mastitic cow is a common source of S. aureus in raw milk [51]. It is widely present in a broad host range, including human beings and food-producing animals, such as pigs, cows, goats, chickens, and ducks [42]. Food contamination with S. aureus may occur directly from infected food-producing animals or may result from poor hygiene during production processes or the retail and storage of food [52].
A multifactorial range of independent risk factors for MRSA has been reported in the literature, and factors include immunosuppression hemodialysis, peripheral malperfusion, advanced age, extended in hospital stays, residency in long-term care facilities, inadequacy of antimicrobial therapy, indwelling devices, insulin-requiring diabetes, and decubitus ulcers, among others [53].
Studies that have been conducted in different regions of Ethiopia indicated the occurrence of S. aureus in food of animal origin as few of them are given in Table 1.
Sample type
No. of examined
No. of positive (prevalence)
Source
Raw bulk milk
168
79 (47)
Enquebaher et al.[51]; Tigray Region, Northern Ethiopia
Naturally soured/fermented raw milk
51
13 (25.4)
Butter milk
44
14 (31.8)
Butter
32
8 (25)
Ethiopian cottage cheese
7
2 (28.6)
Cheese
4
2 (50)
Cakes made from milk
4
2 (50)
Total
310
120 (38.7)
Abattoir
384
36 (9.4)
Adugna et al. [54]; Addis Ababa city
Butcher
384
76 (19.8)
Cutting table
40
6 (15)
Hook
40
6 (15)
Knife
40
9 (22.5)
Total
888
133 (15)
Raw cow milk
170
48 (28.2)
Tessema and Tsegaye [39]; Alage Atvet College Dairy Farm, Ethiopia
Raw cow milk
140
45 (32.14)
Tessema [55]; Wolayta Sodo
Milk shop
86
20 (23.26)
Abraha et al. [43]; Mekelle town
Dairy milk
86
23 (26.74)
Total
172
43 (25)
Milk and milk products
291
68 (23.4)
Ayele et al. [56]; Sebeta
Milk
183
28 (15.3)
Regasa et al. [57]; Mukaturi and Sululta town, Oromia Region
Milk
160
78 (48.75)
Daka et al. [58]; Hawassa area
Beef carcass swab
400
137 (34.3)
Hassan et al. [59]; Asella
Raw camel milk
384
44 (11.45)
Serda et al. [60]; Jigjiga district