Staphylococcus aureus infections

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Identity

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Preferred Scientific Name

• Staphylococcus aureus infections

International Common Names

• English: agalatiae mastitis-metritis syndrome; avian staphylococcal infections; bacterial chondronecrosis with osteomyelitis in broiler chickens; bacterial endocarditis in ruminants; bovine actinobaccillosis; comb necrosis in layer breeder chickens; enzootic calf pneumonia; folliculitis of sheep; gangrenous dermatitis of chickens and turkeys; goat mastitis due to staphylococcus aureus; impetigo of sheep; mammary abscess in pigs; mastitis; mastitis in ewes due to miscellaneous bacteria; ovine and bovine infectious keratoconjunctivitis; ovine interdigital pouch lameness; purulent osteomyelitis; pyoderma of sheep; scalded skin disease; septicemia of lambs or kids, tick pyemia; staphylococcal dermatitis; staphylococcal dermatitis in birds; staphylococcal dermatitis in cattle, impetigo, folliculitis; staphylococcal dermatitis, folliculitis, furunculosis, impetigo, of sheep; staphylococcal dermatitis, folliculitis, impetigo, of sheep; staphylococcal mastitis; staphylococcal, staphylococcus aureus, mastitis in cows; staphylococcus aureus mastitis in ewes; Staphylococcus aureus-induced septicaemia; staphylococcus infections in birds

Local Common Names

• Norway: hva; mastitt

Pathogen/s

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Overview

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History

The early classical historical, but un-referenced, description of Micrococcus (Staphylococcus) was recorded by Merchant and Parker (1967). These authors stated that micrococci were first discovered, in pus, by Ogston in 1881, who then divided the organism (Micrococcus) into two other groups namely Staphylococci and Streptococci respectively in 1883.

Merchant and Parker (1967) further stated that in 1884, these organisms (Staphylococci and streptococci) were first cultivated in artificial medium. During this process two species of Staphylococci, Staphylococcus pyogenes aureus and Staphylococcus pyogenes albus emerged.

Scientists have demonstrated the relationship of these cocci organisms to human infections following experimental self-inoculations.

Taxonomy and Nomenclature

Migula, in 1895, officially assigned three organisms (two staphylococci and one streptococci) to the genus Micrococcus and they were then named Micrococcus aureus, albus and citreus respectively in 1900. Further nomenclature of staphylococci into chromogenic strains such as S. pyogenes albus (a non-pigmented variety), a golden form, and an intermediate yellowish variety of S. pyogenes citreus, was observed to be merely a physiological characteristic that was readily lost during primary and sub-cultures. Transformation in historical nomenclature occurred then, when Buchanan, in 1911, used the genus name Micrococcus for the group and later Staphylococcus in 1917.

The first well defined systematic classification of these genera was by Bergey in (1948), who maintained the genus name Micrococcus; and in the 1957 edition classified them in the genus Staphylococcus and family Micrococcaceae consisting of four genera, Planococcus, Stomatococcus, Micrococcus and Staphylococcus. Bergey has since classified Staphylococcus in the family Staphylococcaceae. More than nineteen species of the genus Staphylococcus are recognized and four groups are clearly distinct, based on deoxyribonucleic acid (DNA:DNA) hybridization analysis. These four groups are S. epidermidis, S. saprophyticus, S. simulans and S. sciuri. Of the large number of staphylococcal species, only three (S. aureus, S. epidermidis and S. saprophyticus) are commonly associated with some human and animal diseases. However, S. aureus, amongst the staphylococcal species is one of the most important causative pathogens in a variety of human and animal diseases.

Association of S. aureus with animal diseases

One of the most economically important diseases caused by S. aureus in dairy animals is mastitis. This is commonly defined as an inflammation of the mammary gland accompanied by physical, chemical, pathological and bacteriological changes in the milk and glandular tissues (Blood and Radostits, 1989; Ameh et al., 1993; Oliver et al., 1999; Apolo et al., 1999; Fitz-Patrick, 2000). S. aureus mastitis in cattle, sheep and goats has serious financial and milk production implications for intensive herds and flocks in the diary industry (Elecko, 1998; Smith et al., 1998; Saratis et al., 1998; Barkema et al., 1999; Sears and Smith, 1999).

In an extensive system of production, multiparous ewes have been shown to have higher milk somatic cell counts compared with primiparous ewes (Lafi et al., 1994). In another study, S. aureus was reported to be the dominant pathogen in clinical cases of mastitis from 145 different breeds of Nigerian goats, as well as from 173 quarter milk samples collected from 297 dairy cows, maintained extensively in Egypt (Shoukry and Shabana, 1997).

The eradication of S. aureus from extensive dairy herds or flocks is more difficult than in intensive systems due to a non-adherence to mastitis control guidelines (Zurzul, 1994). Persistence of this organism in affected udders results in poor milk production, low condition scores, culling and preponderance of resistant strains in affected animals (Elecko, 1998; Zecconi and Piccinini, 1999; Tyagunenko et al., 1999; Costa et al., 2000). It can also lead to zoonotic transmissions from milk to man (Blood and Radostits, 1989; Oboegbulem and Fidelis, 1996).

S. aureus has also been incriminated, or shown to be associated with a variety of human and animal diseases. It has been reported as causing a generalized scalded skin disease in lambs, resembling ‘scalded skin syndrome’ of man. The characteristic lesions of this disease include exfoliation with deep ulcerations in the affected areas (Scott and Murphy, 1997; Yeruham et al., 1999).

Other infections caused by S. aureus and reported in pigs, include purulent osteomyelitis with lesions located at the costo-chrondral junction of affected pigs (Jensen et al., 1999). This disease has been experimentally reproduced when eight calves were intramedullarly infused with a haemolytic strain of S. aureus. This induced traumatic osteomyelitis shown by arteriographic and radiographic analysis. The analysis clearly indicated areas marked by an increased sprouting of osteomyelitic arterial networks around the meta-tarsal bones (Das et al., 1998). Similar microscopic osteo-myelitic lesions have also been observed in experimentally infected goats (Hoque, 1997; Singh et al., 1998).

Staphylococcal dermatitis in some domestic animal species is associated with three bacterial species, S. aureus, S. hyicus and S. epidermidis. S. aureus induced septicaemia has also been reported in chickens and lambs (Pyrah et al., 1994; Rasmaswamy et al., 1997; Fisher et al., 1998). Other important diseases associated with S. aureus in domestic animals which have serious implications in intensive and extensive husbandry systems includes agalactiae mastitis-metritis syndrome in cows and pigs. This is characterized by a purulent uterine discharge (Aerts et al., 1995; Esmat and Badr, 1996). Other equally important diseases implicated or associated with S. aureus in domestic animals are: ovine interdigital pouch lameness (Egwu et al., 1994), bovine actinobaccillosis (Mondodori et al., 1994), abcessation (Sharma et al., 1994), porcine gastroenteritis (Ayoade et al., 1990) and ovine/bovine infectious keratoconjunctivitis (Egwu et al., 1989; Egwu, 1992; Egwu et al., 1993; Chhabra et al., 1996; Takele et al., 2000).

The ability of S. aureus to produce these diseases in domestic animals, is due to elaboration of cytolytic, sphingomyelinase, leukocidic, demonecrotic and entero-toxins (A-E). These include enzymes such as hyaluronidase, nucleases, penicillinase, sphingomylinase, coagulases and the production of ‘slime’, which is known to aid attachment, inversion and multiplication of the organism (Baselga, 1994).

Drastic reduction and elimination of S. aureus-induced diseases, particularly mastitis, should involve good management. This includes good housing, sanitation, maintenance of milking equipment, routine monitoring and surveillance, composite and bulk milk testing, milker's hygiene, accurate timing and strategic treatment or chemotherapy of all diseases induced or associated with S. aureus. These measures are important to ensure the production of good quality milk and profitability. More importantly they are ensuring the consumption of high quality milk as one of our essential dietary components, with reduced chances of contracting diseases such as tuberculosis, streptococcal sore throat, staphylococcal entero-toxin and brucellosis. These are all of zoonotic importance, and are commonly associated with inadequate food safety or hygiene.

Host Animals

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Hosts/Species Affected

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Vectors and Intermediate Hosts

No vectors or intermediate hosts are needed for the development or transmission of S. aureus, and perhaps other staphylococcal organisms. Moreover, no literature exists to date reporting any significant role vectors or intermediate hosts may play in the transmission of staphylococcal diseases.

Hosts

There is a wide host range for infections caused by S. aureus and other important specific diseases caused by this species. Nevertheless, host susceptibility is dependent on a number of factors.

Survival of the causal organism in different climatic and geographical locations may depict differences in invasiveness, virulence, pathogenicity and therapeutic variations as observed with this species (Blood and Radostits, 1989; El-Sukhon, 1995; Bansel et al., 1995; Mackie et al., 1998; Zadoks et al., 2000; Larsen et al., 2000).

Host specific influences, such as whether the animal is at the primiparous or multiparous state, can influence the colonisation, distribution and transmission of S. aureus in all clinical stages of mastitis (Blood and Radostits, 1989; Pyorala et al., 1994; Simpson et al., 1995; Poornima and Updhye, 1995; Boscos et al., 1996; Vural et al., 1999).

The age of the female animal is also an important consideration in the susceptibility to mastitis, as the number of pregnancies can affect intramammary infections (Blood and Radostits, 1989; Vural et al., 1999). Some inherited genetic characteristics, or resistance conferred by the host in retarding the entry and penetration of S. aureus into tissues of the udder, can be reflected in the anatomical conformation. This includes the size of the udder, shape, length of the teat and the openings of the teat sphincter (Blood and Radostits, 1989; Saratis et al., 1998; Aliyu et al., 1999).

Variations in the breed susceptibility of dairy animals to mastitis and other staphylococcal infections have been reported (Blood and Radostits, 1989; Egwu et al., 1995a; Boscos et al., 1996). Extensive dairy husbandry and semi-intensive systems, particularly in tropical countries during the time of scarce pasture grazing, result in various injuries of the teat. These injuries include abrasions, perforations of the udder and dog bites resulting in jagged and lacerated wounds, which enhance fast entry of the causal mastitis organisms (Smith and Roquisnsky 1977; Ameh et al., 1993, Lafi et al., 1998).

Host immunity may involve the ability of the animal to mount an effective systemic and local immune response. This is an important aspect of the host susceptibility to infection. Production of antibodies to specific immunogenic epitopes of S. aureus and cellular immune responses could determine the ability of the host to ward-off previous or recent infections by S. aureus and other staphylococcal diseases (Blood and Radostits, 1989; Park et al., 1999; Hayakawa et al., 2000; Rivas et al., 2000; Riolett et al., 2000).

Systems Affected

Top of page blood and circulatory system diseases of large ruminants
blood and circulatory system diseases of pigs
blood and circulatory system diseases of poultry
blood and circulatory system diseases of small ruminants
bone, foot diseases and lameness in large ruminants
bone, foot diseases and lameness in pigs
bone, foot diseases and lameness in small ruminants
digestive diseases of large ruminants
digestive diseases of pigs
digestive diseases of poultry
digestive diseases of small ruminants
mammary gland diseases of large ruminants
mammary gland diseases of pigs
mammary gland diseases of small ruminants
multisystemic diseases of large ruminants
multisystemic diseases of pigs
multisystemic diseases of poultry
multisystemic diseases of small ruminants
muscular skeletal diseases of poultry
nervous system diseases of large ruminants
nervous system diseases of pigs
nervous system diseases of poultry
nervous system diseases of small ruminants
reproductive diseases of large ruminants
reproductive diseases of pigs
reproductive diseases of poultry
reproductive diseases of small ruminants
respiratory diseases of large ruminants
respiratory diseases of pigs
respiratory diseases of poultry
respiratory diseases of small ruminants
skin and ocular diseases of large ruminants
skin and ocular diseases of pigs
skin and ocular diseases of poultry
skin and ocular diseases of small ruminants
urinary tract and renal diseases of large ruminants
urinary tract and renal diseases of pigs
urinary tract and renal diseases of poultry
urinary tract and renal diseases of small ruminants

Distribution

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Staphylococcus aureus and the diseases this organism causes, or is associated with, occur worldwide in all continents and countries of the world. Surveys of various incriminated infections and diseases have shown remarkable similarity in epidemiology of S. aureus and its associated diseases (Blood and Radostits, 1989; Ameh et al., 1993; Oliver et al., 1999).

Although the distribution and occurrence of S. aureus and its diseases as shown on the map, the geographical spread is not exhaustive. The organism is widespread in countries where intensive and extensive livestock rearing are prominent (Smith et al., 1998; Blood and Radostits, 1989; Barkema et al., 1999).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Last updated: 10 Jan 2020

Pathology

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Gross pathology

Gross and histopathological changes are common features that are associated with mastitis infected glands. Gross lesions are usually obvious following palpation of the infected udder and can be either a result of pronounced or massive swellings. The udder is usually enlarged to approximately twice its normal size, with other associated signs which are discussed in the disease course text (Blood and Radostits, 1984; Egwu et al., 1994; Ameh et al., 1996; Fabre et al., 1997). Necrotizing gangrenous lesions are a common feature associated with mastitis caused by S. aureus, Clostridium perfringens and Escherichia coli (Blood and Radostits, 1989; Ameh et al., 1994). The affected gland shows marked necrosis of the parenchymal epithelium coupled with foci of epithelial erosions, and ulcerations of the ductal system and surrounding skin (Blood and Radostits, 1989; Ameh et al., 1994; Cifrain et al., 1995, Jones, 1998).

Though necropsy procedures are usually not common in animals that have died of gangrenous and other clinical forms of mastitis, further examination of histopathological changes in affected animals are important in order to ascertain the extent of tissue damage.

Histopathology

Lesions observed through histopathology, include accumulation of large numbers of PMNs and other inflammatory cell cytokines (Sanchez et al., 1994; Shoshani et al., 1995; Leitner et al., 2000). Histologically, the inter-lobular duct’s epithelium, in the infected mammary gland, has been displaced by bits of necrotic debris and bacterial clumps. These ducts (interlobular) are necrotic with fibrinous thrombi, and sometimes the vascular walls of the inter-lobular stroma exhibit thrombosis (Shibahara and Nkamura, 1999; Leitner et al., 2000).

Marked accumulation of PMNs, which is sometimes not reflected in the grossly affected gland, is the basis of sub-acute diagnosis of mastitis using the California, Wisconsin and other somatic cell counts (Lam et al., 1996; Hulsen, 1997). This histopathological change, though not diagnostic for S. aureus-induced mastitis, could reveal the causative agent of the mastitis pathogen if backed by a laboratory culture of the collected samples.

Diagnosis

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History of Persistent Mastitis

This forms an integral part of the diagnostic tool of staphylococcal mastitis. A history of recurring and persistent mastitis in a flock or herd probably involves S. aureus as the sole or one of the multi-causative agents. This is because S. aureus can produce resistance to most anti-bacterials, as a result of production of beta-lactamase or penicillinase, allowing the organism to persist in the tissues of the udder (Allen et al., 1994; Simko and Bartko, 1996; Schlegelova and Sediva, 1999) following prolonged antibiotic treatment with unsuitable antibiotics.

Diagnosis based on history can be carried out either during on farm investigations/visits or by the use of questionnaires. Questions asked are usually based on the number of animals affected in the flock or herd, morbidity and mortality, breed, recurring cases, milk yield etc. Response to antibiotic treatments, cure rates and hygiene practices should form the bed-rock of using history as a diagnostic tool during epidemiological investigations.

Clinical Signs

The gross clinical signs manifested in affected animals with mastitis are very obvious, even when accompanied by systemic infections. Since many clinical forms of the disease have been described by many authors (Blood and Radostits, 1989; Deutz et al., 1995; Ameh et al., 1996; Fabre et al., 1997), most farmers can recognize affected animals with mastitis grossly or following assistance by veterinarians. Early recognition of these forms of mastitis allows urgent and prompt action for the affected animal, including initiation of treatment where necessary.

Laboratory Diagnosis

Laboratory diagnosis forms another very important component for confirmatory diagnosis of S. aureus mastitis and related diseases. The colony morphology on simple laboratory media may be fundamental in ascribing the agent S.aureus as a causal organism from cultured samples, particularly for sheep and ox-blood agar plates, due to the production of alpha or beta haemolysis. Laboratory cultures of milk from individual quarter, half, composite or bulk tanks, can be used to enable isolation of the organism (Hogenveen et al., 1997; Leitner et al., 2000). Cows, ewes, does and other animals with sub-clinical mastitis, may pose serious diagnostic problem(s) to the inexperienced farmer. Somatic cell and bacterial counts are then needed to make an accurate diagnosis (Blood and Radostits, 1989; Simpson et al., 1995; Hulsen, 1997; Lam et al., 1996) based on the degree of inflammatory PMNs and the number of leukocyte cells detectable on a graded scale.

Bacterial counts of more than 200 are used as a baseline for positive samples (Blood and Radostits, 1989). Somatic cell counts (PMNs) greater than 250,000/ml in milk are suggestive of an inflammatory process (Blood and Radostits, 1989; Beloti et al., 1997; Barkema et al., 1997; Allore et al., 1998; Bauldry et al., 1999). Examination of milk using the milk cup, in the laboratory or by the pen-side of the affected animal, is important for enabling the farmer, veterinarian or technologist to assess the milk quality, by examining the consistency and colour of the milk. Also important is the combined use of somatic cell count and N-acetyl-beta-D-glucosaminidase (Ngase) enzyme in discriminating the quarters with or without mastitis (Faingold et al., 1995; Pyorala and Pyorala, 1997). Experience and practice with any of these procedures highlighted will assist in the diagnosis and recognition of mastitic milk.

Serology

Mastitis caused by S. aureus is increasing in importance throughout the world. Since intensification of dairy farming, even in some tropical countries, the disease is gaining recognition, and therefore the control and eradication of mastitis should be of utmost priority to the dairy farmer. Early diagnosis of this disease using more reliable, specific and sensitive laboratory diagnostic tools, is gaining acceptance for rapid prevention and initiation of chemotherapeutic measures. Strains of S. aureus may vary in their geographical origin and antibiotic sensitivity patterns, as well as in their phage or ribotypes (Aarestrup et al., 1995; Adesiyun, 1995; Yoshida et al., 1997; Raimundo et al., 1999). Furthermore, diverse geographical isolates of S. aureus can be characterized by using genomic finger printing of isolates from milk. In one such study, 137 S. aureus isolates were categorized into 20 distinct DNA finger printing profiles, which were further amplified by PCR at 506, 770, 784 and 2479 bp regions (Kim et al., 1999). Also the use of genes expressed by S. aureus have been amplified using PCR on milk samples (Khan et al., 1988; Lammers et al., 2000; Tisala et al., 2000). Example genes used are the ‘nuc gene’ or those screened from the mutant library (Lac Z mutants), including those from the 165-235 ribosomal RNA spacer sequences. Other combined diagnostic techniques incorporating laboratory culture, somatic cell counts and enzyme linked immunosorbent assays have been described for the diagnosis of S. aureus mastitis in dairy cows (Hicks et al., 1994; Fox and Adams, 2000). Some other laboratory sensitive methods for the diagnosis of diseases caused by S. aureus, include the use of pulse field gel electrophoresis for identification of isolates (Mc Cullagh et al., 1998; Dalamitra et al., 1998) and other simple laboratory enzyme-based methods for milk samples (Faingold et al., 1995; Pyorala and Pyorala, 1997).

Immunology

Systemic and local immune responses are provoked during intra-mammary infection with S. aureus. The immunoglobulins involved in body fluids or milk during humoral immunity are IgG1, IgG2, IgG3, IgA and IgMs (Guidry et al., 1994; Leitner et al., 2000). As a result of possession of different antigenic components on the surface of S. aureus, antibodies are usually directed against these surface antigenic sites, and to the different toxins elaborated by these organisms (Baldi et al., 1994; Quinones and Demo, 1997; Jones, 1998).

Cellular immunity also plays a functional protective role in S. aureus mastitis and other staphylococcal diseases. Specific recruitment of mammary neutrophils and leukocyte or lymphocyte sub-populations following vaccination with type-5 capsular polysaccharide (Cp5) antigen and whole cells of S. aureus, have been reported in experimental studies (Herbelin et al., 1995; Almeida et al., 1997; Waller and Colditz, 1999). Nevertheless, altered immune reactions such as type I hypersensitivity reactions following inoculation of S. aureus have been reported in an experimental goat (Schofield et al., 1997). This shows that immunology to this disease can be protective, but can sometimes be accompanied by altered states of immunological reactions, which can be damaging to the affected host.

List of Symptoms/Signs

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Disease Course

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Pathogenesis

S. aureus induces disease by either toxin production (Cifrian et al., 1996; Quinones and Demo, 1997; Jones 1998), or by direct invasion and destruction of tissues (Kang et al., 1996; Quinones and Demo, 1997).

Other staphylococcal species can invoke disease by proliferation of the causative agent in conjunction with some virulent toxins and/or associated enzymes produced by these organisms (Blood and Radostits, 1989; Baselga, 1994; Bezek and Hull, 1995; Ichikawa 1996). Amongst the numerous diseases caused by S. aureus, mastitis is of a high priority in dairy animals. This disease (mastitis) can be classified as per-acute, sub-acute, acute and chronic (Blood and Radostits, 1989; Simpson et al., 1995; Topolko and Benice, 1997) forms or clinical stages.

The disease process is dependent on the ability of the organism (S. aureus) to survive in the vicinity of the dairy animal, and its ability to confer resistance on a variety of disinfectants and antibiotics used in the farm (Boddie and Nickelson, 1997).

The strain variation of S. aureus accounts for the degree of pathogenicity (Bansal et al., 1995; Hermans et al., 2000). However, the size of the inoculum, stage of lactation, injuries on the teat and elaboration of toxins and enzymes will determine the type of mastitis and pathology induced in the hosts (Sultra and Poutrel, 1994; Bansal et al., 1995; Ameh et al., 1993; Quinones and Demo, 1997; Fitzgerald et al., 2000). In spite of these aforementioned factors, the adherence of S. aureus to the epithelial cells of the mammary gland, is the first process required for the initiation of pathogenesis (Katic et al., 1996).

Clinical Forms of Mastitis

Per-acute

This occurs most frequently during infections of early lactation (Blood and Radostits, 1989). It is sometimes accompanied by gangrene of the udder, due to the necrotizing action of the alpha toxins (Cifrain et al. 1995; Jones 1998). Per-acute mastitis usually occurs during the first few days of lactation and is accompanied by a severe temperature elevation to 41 - 42^°C, tachycardia, pronounced depression, absence of rumen motility and muscular weakness (Blood and Radostits, 1989). The affected quarter or half of the animal is swollen and hard. There is subcutaneous emphysema, blister formation and gangrene in some affected cases. These inflammatory processes can subside within a few days, and the infected gland is then replaced by proliferation of connective tissue, marked by blockage and atrophy of the ductal area.

Sub-acute

The sub-acute form of S. aureus mastitis is transient and mimics the clinical signs of either the acute or chronic forms, or both. The milk may show some degree of infection as evidenced by blood clots (Blood and Radostits, 1989; Petrovic et al., 1997) with an elevation of the leukocyte counts (Lam et al., 1996). The California mastitis test (CMT) is routinely used on individual, composite and bulk milk samples (Simpson et al., 1995; Leitner et al., 2000) to detect levels of polymorphonuclear cells (PMNs). The temperature of the affected animal may or may not become elevated (Blood and Radostits, 1989; Egwu et al., 1994; Rapoport et al., 1994).

Acute

The acute form of mastitis is characterised by a visible enlargement of the udder. There are marked changes in the milk observed, such as evidence of blot clots, fibrin, watery consistency, lobules and coloration. The temperature of the animal is elevated and the enlarged udder is painful on palpation. The affected animal is weak, comatose and sometimes becomes recumbent in unfavourable situations (Ameh et al., 1996; Fabre et al., 1997). Other associated signs include dullness, anorexia, inappetence and general malaise. Milk quality and production are reduced drastically (Wilson et al., 1997). This form is clinically recognizable by the farmer and provides an opportunity for reporting such cases urgently to the veterinarian or other appropriate authorities.

Chronic

If an animal is suffering from the chronic form of mastitis, the functional capacity of the udder is compromized. There is atrophy or shrinkage of the udder and milk production is also drastically reduced. The glandular tissue becomes fibrosed, and sometimes the ducts are blocked with difficulty in milk letdown through the teat sphincter (Shoshani et al., 1995). Most causal agents persist in the udder during this stage and with appropriate treatment, recovery from this clinical form of mastitis is high (Deutz et al., 1995). Farmers usually try to maintain patency of the teat canal by making use of teat cannulas. Total milking out by farmers or veterinarians can assist in the successful application of chemotherapy at this stage.

Epidemiology

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The staphylococcal species, with particular reference to S. aureus and associated diseases, are ubiquitous worldwide and affect a whole range of domestic and wild animals (Blood and Radostits, 1989; Oliver et al., 1999; Smith 1999).

S. aureus is always a dominant causal agent of mastitis (Smith et al., 1998; Elecko, 1998; Oliver et al., 1999) and is also highly predisposed to many organs of animal and human hosts, thereby causing different diseases (Egwu et al., 1989; Mondodori et al., 1994; Esmat and Badr, 1996; Ramaswamy et al., 1997; Takele and Zerihun, 2000).

Direct replication (cell division) of S. aureus is by binary fission and intermediate hosts or vectors are not necessary in the development of this organism. However, it is interesting to note that tick-pyaemia of lambs, characterized by elaboration of neuro-toxins, as a result of tick bites on the definitive host (lambs) is enhanced by S. aureus (Clarkson and Faull, 1985; Blood and Radostits, 1989). The obvious lesions resulting from these septicaemic staphylococcal infections are lameness, abcessation of vital organs, unthriftiness and general weakness of affected lambs. Experimentally, ixodes ricinus ticks acting as intermediate hosts infected with S. aureus have also reproduced typical lesions of tick pyaemia (Webster and Mitchell, 1986). The disease (tick pyaemia) has been reported as occurring naturally and concurrently with other diseases of domestic animals such as, enterotoxaemia, tick-borne fever, louping ill and lamb dysentry (Clarkson and Faull, 1985; Blood and Radostits, 1989).

Incubation Period and Transmission

The primary barrier protecting against the entry of S. aureus into the mammary gland is the teat sphincter. When the pathogen (S. aureus) overcomes this barrier, if not washed out by the physical act of milking, the bacteria multiplies, invades and proliferates in the udder tissue (Das and Khanna, 1994; Sultra and Poutrel, 1994).

Considerable variation occurs amongst susceptible animals, between infection and appearance of clinical signs. The incubation period may be for 3 - 4 days following infection of the teat (Blood and Radostits, 1989; Fox et al., 1995), with inflammatory processes coming into action 3 - 5 days later. These processes however, depend on the virulence, host immune mechanisms and weight of infecting pathogen. These factors also determine the degree of pathology and type of mastitis produced (Blood and Radostits, 1989; Das and Khanna, 1994; Sutra and Poutrel, 1994; Bansel et al., 1995).

Direct and indirect transmission of S. aureus, are usually the main avenues of disseminating an infection. Usually, mammary gland infection occurs via the teat canal and/or environment (Blood and Radostits, 1989; Bansal et al., 1995; Bouchard et al., 1996; Kosev et al., 1996). It can also occur through other unhygienic measures such as, housing, defects in milking machines and management factors (Demchonko, 1994; Vasil, 1994; Refsdal, 1996; Fox et al., 1995; Benda 1998; Barkema et al., 1999). Other inter-alia factors include: the use of clean milking towels for pre and post cleaning of mammary teats, clean calving pens, unhygienic housing condition, improper adjustments of milking machine, dirty teat cups or the use of unclean hands during hand milking. The importance of all factors mentioned cannot be overemphasized in their respective roles in the transmission of mastitis pathogens.

S. aureus is known to co-exist with many other bacterial pathogens occurring in the environment and other animal sites (Poorima and Updhye, 1995; Poorima and Upadhye, 1995; Huan and Huan, 1996; Yanni, 1999). However, the ability of S. aureus to persist in the tissue of the udder makes it somewhat more ameliorable to treatment, compared to other organism such as Escherichia coli, Streptococcus dysagalactiae, S. uberis and Pseudomonas aeruginosa that are all found in the environment (Sultra and Poutrel, 1994).

Since S. aureus is ubiquitous in distribution and is also involved in many other animal diseases, contact transmission, aerosol transmission, wounds and abrasions on the body surface play an important role in the transmission of S. aureus (El-Sukhon 1995; Poorima and Upadhye 1995; Yanni, 1999; Moller et al., 2000). They also play a role in other induced diseases such as mastitis-metritis syndrome, abcessation, gastroenteritis, septicaemia, osteomyelitis and urinary infections, including respiratory and environmentally acquired infections. Dissemination of the organism from one organ to the other is also possible, depending on the invasiveness or multiplication of the organism in the host tissues.

Impact: Economic

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Economic impact of Mastitis

Mastitis caused by Staphylococcus aureus, is a major disease for the dairy industry to contend with, if productivity and health of the animals are to be ensured.

Generally in most affected animals, losses occurring from fatalities amongst dairy herds are very minimal compared to those resulting from milk production (Blood and Radostits, 1989; Deutz et al., 1995). Affected cows with sub-clinical mastitis have been shown to produce low birth weight calves (Dominigues et al., 1996). This may pose very serious economic costs and returns in rearing the dairy calves.

Contaminated milk has transmitted some zoonotic bacteria to man, when the milk has not been properly pasteurized before human consumption. Such diseases caused by this transmission include tuberculosis, streptococcal sore throat, brucellosis and staphylococcal food poisoning (Blood and Radostits, 1989; Mousing et al., 1997; Hernandez and Baca, 1998). Most of these diseases are becoming devastating in most developing countries and some are emerging as diseases in parts of the developed world.

Economic effects resulting from quarter or udder half infections of the mammary gland are drastically reduced milk yield, monetary returns and profit to the dairy farmer. This is dependant on the stage of lactation and time of infection (Shoshani et al., 1995; Deutz et al., 1995; Ameh et al., 1996; Fabre et al., 1997). Infection of cows during the dry period could reduce milk yield by up to 11%, whereas those occurring at late lactation could reduce percentage yield by up to 48% (Blood and Radostit, 1989; Deutz et al., 1995). This constitutes tremendous economic waste and financial returns to the dairy farmer.

The prevalence of specific mastitis pathogens such as S. aureus varies from herd to herd. In a high prevalence herd, conservative economic milk losses resulting from S. aureus mastitis on a ‘cow basis’, could be in excess of US $90-250, particularly in large dairy herds (Blood and Radostits, 1989).

Quarters or halves of udders from animals infected with S. aureus, alone or in combination with other mastitis pathogens, can result in low or poor quality milk and market sales (Shoshani et al., 1995; Lam et al., 1996; Fabre et al., 1997). Losses emanating from premature culling as a result of unthriftiness or poor condition of acutely or chronically affected animals, could seriously undermine the productivity of the dairy farm as well as monetary returns (Deutz et al., 1995; Dominigues et al., 1996; Moclerson et al., 2000).

The greatest economic losses for dairy farms with mastitis are usually associated with the costs of veterinary medicine and care, particularly in those herds with acute or chronic forms of the disease. The use of pre-dipping disinfectants, intra-mammary antibiotics and other systemic antibiotics can impact large economic losses in monetary terms to the dairy farmers. This is especially the case, if these are carried out routinely in the process of trying to eliminate persistent and recalcitrant strains of S. aureus on a dairy farm.

Apart from those practices aimed at reducing intra-mammary infections, there are other diagnostic costs incurred by the farmer. These include routine somatic milk counts on individual, composite and bulk milk samples and the increased labour costs for this. There are obvious advantages in monitoring levels of milk infection, but it does create an extra cost.

Other Economic Impact of S. aureus Associated or Induced Diseases

Other losses occurring from S. aureus induced or associated diseases, include blindness in small and large ruminants. This could be temporary or permanent blindness as observed in sheep, goats and cattle suffering from ovine, caprine and bovine kerato-conjunctivitis (Egwu et al., 1989; Al-Gaabary et al., 1998; Takele and Zerihun, 2000). Affected animals with this acute or chronic ocular disease are unthrifty, off-feed, emaciated and generally lose sight of their environment. It is not clearly known what role S. aureus plays in initiating the disease or exacerbating the disease condition, but its frequent association with the disease process is likely to indicate a possible role of toxins and enzymes, and other ocular inflammatory mediators in the disease process. Corneal ulceration (see picture) which is usually purulent, or scarification on the cornea following healing, has been reported to be associated with S. aureus following natural and experimental infections (Egwu et al., 1989; Egwu and Faull, 1991, Egwu and Faull, 1993).

Tick pyaemia causes the early death of lambs, particularly those with good traits that make them potential replacements for breeding ewes. Losses from this disease could be as a result of septicaemia, lameness, arthritis and disseminated abscessation of vital organs (Clarkson and Faull, 1985; Webster and Mitchell, 1986).

Zoonoses and Food Safety

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There is an important public health aspect of S. aureus infections. Staphylococcal food poisoning is becoming important in the milk and meat industry (Blood and Radostits, 1989; Mousing et al., 1997; Hernandez and Baca, 1998). Nosocomial (hospital acquired) infections are common sources of acquiring S. aureus. The need for pasteurization of milk before consumption, and the sterilization of prosthetic surgical equipment before open surgery must also be ensured. Many other pathogens of zoonotic importance apart from S. aureus are involved in ‘mastitides’ (Blood and Radostits, 1989). These include Mycobacterium spp. (El-Haenaeey et al., 1994; Klinger and Rosenthal, 1997), and commonly incriminated species of this genera (mycobacterium) include: M. bovis, M. fortuitum, M. smegmatis, all of which are commonly acquired from contaminated milk and its products. Infections can also be obtained from infections of the hosts or from contaminated unhygienic preparations of milk and meat products (El-Haenaeey et al., 1994; Klinger and Rosenthal, 1997). Clostridium perfringens type A, Bacillus spp., Campylobacter jejuni, and Brucella abortus and milletensis are also commonly acquired pathogens from improperly pasteurized milk and its products (Egwu et al., 1994; Huan and Huan 1996; Waage et al., 1999).

The isolation of S. aureus from local milk products (nono) or local yoghurts, even at low pH has been reported by Egwu et al. (1995b). Consumers should therefore ensure that milk and meat products are wholesome before taking them to market, to ensure freedom from some of these zoonotic diseases. This is particularly important in developing countries where consumption of local milk products is popular.

Disease Treatment

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Consideration for the treatment of S. aureus induced diseases should involve the target sites involved in the disease process. These sites include the udder, respiratory tract, eyes, bones and skin where the diseases are manifested. Priority is however ascribed to S. aureus mastitis, as it stands out prominently because of the economics involved in controlling the disease. Treatment should aim at combating or controlling the severity of mastitis through chemotherapy, with the use of the right antibiotics following adequate sensitivity tests or anti-biogrammes (Sandgren and Ekman, 1996).

Antibiotics

A number of first generation antibiotics including penicillins, streptomycin, cloxacillin, penicillin/streptomycin combination and nitrofurazone, have been used at various doses and regimens for the treatment of S. aureus mastitis (Blood and Radostits, 1989; Owens et al., 1997; Egwu et al., 1994; Dhabele et al., 1997; Schlegelova and Sediva, 1999).

The intramammary and/or systemic routes are usually employed during the chemotherapy of mastitis (Egwu et al., 1994; Pyorala and Pyorala, 1994; Dhabele et al., 1997; Owens et al., 1997).

Most drugs used in the treatment of S. aureus mastitis tend to be more sensitive in vitro than in vivo (Egwu et al., 1994; Owens et al., 1994; Dhabele et al., 1997), following experience from laboratory and field investigations.

The increasing incidence of S. aureus resistance following mastitis treatment has resulted in inefficacy treatment in the use of antibiotics (Allen et al., 1994; Simko and Bartes, 1996; Schlegelova and Sediva, 1999).

There is a need for antibiotic sensitivity testing prior to treatment of mastitis to determine the best drug of choice (Cruz et al., 1997; Kumajock et al., 1999). This should involve serum blood concentrations of the drug of choice, minimum inhibitory concentration studies and disk sensitivity antibiotic testing (Owens et al., 1994; Egwu et al., 1994; Allen et al., 1994; Simko and Bartes, 1996), so as to allow the veterinarian to select the best antibiotics.

Ethnoveterinary Practice

Ethnoveterinary practice has not assumed any significance in recent times for the treatment of mastitis and other related diseases. However, the efficacy of this method of treatment has not been properly assessed in line with current antibiotic usage. This practice in nomadic pastoralism could offer some benefits to the nomadic farmer, who may find costs of modern antibiotic treatment very exorbitant. Some of these practices may be handed from generation to generation in the family line.

Chemotherapy of Other S. aureus Diseases

Infections like osteomyelitis, keratoconjunctivitis, and staphylococcal dermatitis can be treated with oxytetracycline, erythromycin, demofloxacin and other suitable antibiotics (Egwu, 1992; Egwu and Faull, 1993; Al-Gaabary et al., 1998).

The commonly used drugs, dose, adverse reactions and possible emergence of resistant strains in the disease treatment table.

Prevention and Control

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Farm Level Control

The pathogenic importance of S. aureus in mastitis and other related infections necessitates the need for its control, eradication and prevention in affected dairy herds (Tichaecek, 1999). Though complete eradication of S. aureus may, to some extent, appear inconceivable or unachievable, the need for continuous monitoring and surveillance in affected dairy herds or flocks cannot be overemphasized.

A holistic approach is therefore needed to achieve a meaningful eradication programme of mastitis that will maximize profitability in the dairy industry.

Awareness of farmers

To raise farmer awareness, there should be an on-farm discussion by veterinarians, animal scientists and dairy epidemiologists, with dairy farmers on the need to be constantly aware of and control this important disease (mastitis). The importance of the ability to recognize the clinical signs of mastitis and the performance of simple routine tests on milk by the farmers, cannot be underestimated. Some of these facets of awareness in the control of mastitis have been previously documented (Majic et al., 1994; Brown et al., 1998). There is a need for farmers to partake in all aspects of the on-farm control measures if the weight of the infecting organisms and elimination of the causal agents are to be achieved in the dairy farm.

Husbandry Practices

Management is important in the control of S. aureus mastitis. The components of this aspect of management include housing, movement of livestock, in-house sanitation of cow cubicles, pens and milking parlours, as well as milking procedures and general hygiene of the milker and premises (Vasil, 1994; Benda, 1998; Barkema et al., 1999).

It is a recognized fact, that the dairy industry is well developed in more temperate than tropical countries. In the latter countries, nomadism and transhumance practices that are tied to the extensive and semi-intensive husbandry have compromized some of the enumerated measures (Smith et al., 1998; Ameh et al., 1993; Aliyu et al., 1999). These practices, rather than enhancing control have worsened it, because animals are usually herded together, eat and drink together and generally disseminate and contract infections.

Housing

It is a known fact, that the construction of dairy houses in temperate region is of a higher quality standard than those in the tropics, where milking animals are always on the move and sedentary herds or flocks are rarely found. Even where dairy farm houses exist, in-house milking equipment and other infrastructures may vary from farm to farm. The hygienic conditions of this equipment and the degree of disinfection in the dairy houses, may account for the prevalence of S. aureus on these farms (Blood and Radostits, 1989; Poorima and Updhye, 1995; Barkema et al., 1999).

The site or location of the house, as well as the nature (wooden or concrete) can significantly affect the prevalence of mastitis pathogens (Poorima and Updhye, 1995; Barkema et al., 1999).

The bedding material used, such as wet sawdust has been shown to easily predispose to mastitis compared to dry shavings and straw (Blood and Radostits, 1989).

Milking parlour/milking cow

The milking parlour should be routinely disinfected and overcrowding during milking minimized. The mammary gland of the milking cow should be washed with a mild disinfectant containing mild and suitable antiseptics. This should include the use of creams and solutions on teat sores, which constitute a common source for entry of bacterial pathogens (Blood and Radostits, 1989; Saratis et al., 1998; Aliyu et al., 1999). Practising pre- and post-dipping of the teat can reduce the incidence of mastitis in the herd, for example the use of 0.25% or 0.5% solutions of providone iodine (hydrochloride) and iodine.

Milking machines

There is no doubt that milking machines constitute an essential component of the infrastructures required in the dairy industry. However, the misuse of these machines has resulted in increased subclinical and clinical mastitis (Vasil, 1994; Refsdall, 1996; Barkema et al., 1999).

Therefore, for good herd health surveillance in dairy farms, examination of the milking machines to detect faults related to vacuum pressure, milk cup pressures, vacuum capacity, pulsation rate, air bleeds and the milking vacuum at the teat-cup to ascertain no blockage of air vents should be carried out. These measures must be ensured in order to meet standards of specification prior to milking (Blood and Radostits, 1989; Fox, 1997; Barkema et al., 1999).

It is however, important to state that some modern technological advancements in the design of milking machines have incorporated automatic milk cup deflectors, which divert refluxed milk from the pipeline, and also automatic milk cup removers to prevent milk accumulation in the cups and reflux into the tanks.

Restriction of Animal Movement

There is a need to restrict movement of dairy herds to neighbouring paddocks. It is important to minimize or prevent contact of affected animals with clean herds. Nevertheless, the practicability of this practice in pastoral nomadism is far from reality (Mech, 1975; Williamson and Payne, 1978; Gefu, 1982). Strict government laws on livestock movement, quarantine and free market livestock trades should be enforced in all their ramifications to prevent S. aureus mastitis epidemics. National and international policy programmes on livestock movement should ensure that animals with clean bills of health should be allowed to cross international boundaries. There should also be a need for dairy monitoring boards, required to censor infected herds/flocks by examination of milk through testing by somatic cell counts of individual, composite, herd, or bulk milk (Blood and Radostits, 1989; Lam, 1996; Hogeveen et al., 1997; Leitner et al., 2000). This process of testing, backed up with culture, can also detect some other serious mastitis causing pathogens, which may be exotic in the importing country.

Culling

Routine monitoring and surveillance of dairy herds and infected milk allows easy identification of animals suffering from mastitis. This ensures that the affected animals are culled from the herd, enabling the dairy farmer to institute good mastitis control measures. Identified animals that are sick with mastitis should be treated and the farmer should ensure that such animals are routinely removed and treated before allowing them back into the herd. This culling process ensures that certain mastitis pathogens not ameliorable to treatment are kept under check.

Vaccines

The use of vaccines for the control of staphylococcal mastitis has not been well documented and its efficacy is not well ascertained. Vaccines prepared using whole cells of S. aureus, sub-units, anti-toxins or targeted against specific anti-inflammatory cells may be promising, if such vaccines are able to invoke protective anti-body levels. Nevertheless, varying degrees of success have been reported in the field following experimental trials on various species of animals (Nordhaug et al., 1994a, b; Fitzpatrick, 2000; Virtala and Nevalainen, 2000).

Although many S. aureus component vaccines are still undergoing experimental field trials, the likely past and future problems, and efficacy on the use of such vaccines has been previously highlighted (Faria et al., 2000; Fitzpatrick 2000).

The vaccines listed in the table are not exhaustive, the potential acceptability of each vaccine and ability to confer immunity in vaccinated animals remains properly assessed (Han-HongRyul et al., 2000; Virtala and Nevalainen, 2000). It is however, important to note that there is yet to be any effective marketable S. aureus vaccine. The potential for producing S. aureus sub-unit vaccines in the present age of deoxyribonucleic acid recombinant research is great, provided such genetically engineered vaccines targeted against immunogenic epitopes can also cross-protect against similarly related pathogenic bacterial organisms causing mastitis.

It is also important that apart from mastitis induced by S. aureus, no available vaccines exist for immuno-prophylaxis of other diseases caused by or associated with S. aureus. Research into these types of vaccine, for other staphylococcal-induced disease, is still in its infancy, but it is hoped that following experimental trials and field success this type of vaccine will become available.

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