Staphylococci in healthy and diseased animals

Journal of Applied Bacteriology Symposium Supplement 1990,71 S-80s

Staphylococci in healthy and diseased animals

L . A . DEVRIESE Faculty of Veterinary Medicine, University of Gent, Casinoplein 24, B-9000 Gent, Belgium

1 . Introduction, 71s 2. Species distribution in different healthy hosts, 71s 3. Species distribution in disease processes, 73s 4. Biotypes and ecovars, 74s 5. Transfer to unusual hosts and zoonotic aspects, 75s 6. Conclusions, 77s 7. References. 77s

1. Introduction

Different animal hosts carry different bacteria. Certain well-known bacterial species occur in several or many different animal host species but the populations associated with different hosts or with different pathological conditions may differ in certain characteristics. Other bacterial species are typi- cally associated with certain animal host species and do not occur in others. These almost general principles are well illustrated by the staphylococci.

The purpose of this review is to show how members of the genus Staphylococcus are associated in many diverse and specialized forms with healthy and diseased farm animals and with the most common pet animals. Reviews on other important aspects of staphylococcal disease in animals such as pathogenesis and immunity, have been published by Adlam et al. (1983), Anderson (1983) and Colditz & Watson (1985).

2. Species distribution in different healthy hosts

The most important associations of staphylococci with farm and pet animals are listed in Table 1. Among these there are some salient peculiarities. The novobiocin-resistant species Staph. sciuri, Staph. lentus, Staph. xylosus and some others dominate on many farm animals but are relatively rare on dogs and cats. Staphylococcus saprophyticus is only rarely isolated from farm animals, dogs and cats. Dogs are almost exclusively colonized by Staph. intermedius. The coagulase-negative staphylococci, which can be found on the hairy skin (Ihrke et al. 1978), are probably not residents. Strains which were considered to be Staph. simulans (Cox et al. 1985; Devriese et al. 1984a) but which were recently described as a new species Staph.felis (Igimi et al. 1989) dominate on cats. They differ from Staph. simulans genetically and in their sensitivity to bacitracin. Staphylococcus hyicus is a common inhabit- ant of the nares and the skin of chickens; Staph. intermedius is never found in these birds but it is found on pigeons.

Most frequently organisms from the nares and unspecified parts of the animal skin have been studied. With few exceptions staphylococcal populations in different body areas have not been compared as they have in humans (see Noble, this Symposium pp. 39S48S). This point merits attention because it may provide clues to the understanding of certain aspects of the pathogenesis of staphylococcal diseases as well as their prevention and treatment. For example Hajek & MarSalek (1969) found a marked difference between Staph. aureus strains from cases of bovine mastitis and those from the nares of cattle. This observation is pertinent in the context of the reservoir(s) of infection of this most important mastitis agent in dairy cows. Are the mastitis strains confined to the udder region in cattle and particularly restricted to the teats? The novobiocin-sensitive species Staph. haemolyticus, Staph. warneri and Staph. epidermidis colonize teat ducts and the teat apex of cows while Staph. haemolyticus and the novobiocin-resistant Staph. sciuri and Staph. xylosus abound on the teat skin

72s L. A . Devriese Table 1. Most important Staphylococcus species associated with

farm and pet animals*

Animal host Novobiocin resistant Novobiocin sensitive

Cattle Staphylococcus lentus Staphylococcus hyicus xylosus aureus cohnii chromogenes

simulans epidermidis haemol yt icus warneri

Pigs

Poultry

Sheep

Goats

Horses

lentus xylosus sciuri

lentus xylosus sciuri cohnii gallinarum

lentus sciuri

lentus sciuri xylosus

equorum sciuri xylosus

hyicus aureus chromogenes simulans hominis

hyicus aureus chromogenes

aureus intermedius

Dogs intermedius

Pigeons interrnedius

Cats felis

* Based on the following references: cattle, poultry, sheep and goats (Devriese et al. 1985); pigs (Devriese et al. 1985 and Shimizu et al. 1987); horses (Devriese et al. 1984b); cats (Igimi et al. 1989).

(Devriese & de Keyser 1980). Similarly Staph. aureus colonizes the teats, especially when small lesions are present, but they are rarely isolated from the skin even when lesions are present (L.A. Devriese, unpublished). Colonization of the teat apex is an important first step in the pathogenesis of staphylococcal and streptococcal udder infections. Strains or species which are unable to colonize this site are less likely to cause udder infections although they may provoke disease and lesions when they are inoculated into the udder quarters. Observations reported by Mamo et al. (1988) indicate that Staph. aureus and coagulase-negative staphylococci isolated from the bovine udder have the ability to bind to tissue matrix and plasma proteins which may be exposed in traumatized or toxin-damaged udder epithelia. Staphylococcus aureus binds fibronectin, fibrinogen and type I1 collagen more effectively than do other staphylococci of the udder. Staphylococcus warneri shows high fibronectin and collagen binding capacity and Staph. chromogenes and Staph. caprae bind a significant amount of collagen. The binding of fibrinogen by the latter three species, all of which are clumping factor-negative, is negligible (Mamo et al. 1988).

Devriese & de Pelsmaecker (1987) found that the anal region is the main site of Staph. interrnedius in dogs. This can be of importance in the treatment and management of severe recurrent pyoderma cases in sensitive (and hypersensitive? see Scott 1978; Wisselink et al. 1988) dog breeds or individuals. The intact skin of dogs does not harbour any Staph. intermedius (White et al. 1983); these bacteria are shed on the haircoat from the anal and nasal carrier sites.

Staphylococci in animals Table 2. Association of different staphylococcal species with disease processes in

animals*

73s

Host Species Main pathological conditions

Cattle

Pigs

Poultry

Turkeys

Ducks

Pigeons

Rabbits

Mink

Sheep

Goats

Horses

Staphylococcus aureus hyicus epidermidis warneri chromogenes hyicus simulans

hyicus aureus

aureus

hyicus

aureus

aureus intermedius

intermedius

aureus

1

intermedius

aureus

epidermidis

aureus epidermidis caprae sciuri

aureus intermedius hyicus

ssp. anaerobius

i

mastitis (clinical and subclinical) secondary skin infections

mastitis (subclinical)

dermatitis, sporadic joint infections sporadic septicaemia

synovitis-arthritis-osteomyelitis,

spondylitis

synovitis-arthritis-osteomyelitis

septicaemia, arthritis septicaemia

sporadic septicaemia

mastitis, exudative dermatitis, abscesses, pododermatitis

dermatitis, urolithiasis

mastitis, dermatitis, lamb pyaemia abscesses (Morel’s disease) mastitis

dermatitis

mastitis

dermatitis and cellulitis

* Selected references: some of the less well-known situations have been reported in the literature as follows: duck infections (Humrnel er al. 1982b); spondylitis in chickens (Devriese 1980); infections in mink (Crandell et al. 1971) and rabbits (Okerman et al. 1984); Staphylococcus aureus subsp. anaerobius in goats (de la Fuente et al. 1985); mastitis with coagulase-negative staphylococci in goats (Poutrel 1984a, b) and sheep (Guitierrez et al. 1982).

3. Species distribution in disease processes

Three major pathogenic staphylococci, Staph. aureus, Staph. intermedius and Staph. hyicus, are of importance in veterinary medicine. The more exotic animals may also suffer from disease due to other, as yet unknown, staphylococci. For example, a new coagulase-positive species from dolphins, Staph. delphini, was recently described (Varaldo et uI. 1988). Other well-known coagulase-negative species of this genus may act as pathogens in animals, but in contrast to humans, these staphylococcal species have received little attention as yet in animals. The main reason for this probably lies in the fact that hospitalization and intensive care of debilitated, geriatric patients is not so widely prac- ticed in general veterinary practice as it is in human medicine. One important, but to date largely unexplored, exception is the role of coagulase-negative staphylococci in subclinical mastitis in ruminants (Holmberg 1986).

The involvement of staphylococci in different disease processes in animals is illustrated in Table 2. In some animal hosts only one species of this genus is of importance whereas in others several species

74s L. A . Devriese are associated with disease. Among the animals of common veterinary interest, the horse is unique in that all three major pathogenic species, Staph. aureus, Staph. intermedius and Staph. hyicus may be found in lesions (Devriese et al. 1984b). The first two are members of the normal equine nasal flora (Hajek et al. 1974) and Staph. hyicus can be involved in certain skin lesions, especially those involving the limbs (Devriese et al. 1983).

The staphylococci associated with lesions in a given animal host usually belong to the endogenous flora of that animal species, but this is not always the case. Staphylococcus aureus and Staph. intermedius are not infrequent in superficial lesions of cats, but they may well originate from humans or dogs. Both Staph. intermedius and Staph. aureus may be isolated from carrier sites in cats, most often from the hair coat, but their residency status is uncertain (Cox et al. 1985). The same question about origin is raised in respect of certain coagulase-negative staphylococci. Staphylococcus epidermidis, the most important coagulase-negative member of the genus in humans, is rare in animals. Indeed Kloos (1980) regarded this species as exclusively human. In some studies (Baba et al. 1980; Devriese 1979; Guitierrez et al. 1982; Poutrel 1984a; Harvey & Gilmour 1988), however, Staph. epidermidis was often found on the teats and in the milk of cows, sheep and goats with subclinical mastitis. These infections may have originated directly from the milkers. Alternatively, in its evolution Staph. epidermidis may have acquired recently an attribute which enables it to colonize and infect udders.

4. Biotypes and ecovars

Following the pioneering work of Meyer (1966kwhich was itself based on many observations of earlier workers-Hajek & MarSalek (1971) proposed a comprehensive scheme for biotyping Staph. aureus. This scheme has proved to be very useful for distinguishing between different biotypes of Staph. aureus and Staph. intermedius. Without modifications or in a more extended form (Witte et al. 1977; Gibbs et al. 1978a; Akatov et al. 1981; Shimizu et al. 1986) or in a simplified form (Devriese 1984), it continues to be used by many workers. Staphylococcus aureus biotypes have been shown to share more than an 80% nucleotide sequence homology without clearcut distinctions under restrictive conditions but lower values were seen with different biotypes of Staph. intermedius (Meyer & Schleifer 1978).

Not surprisingly most biotype distinctions have been concerned with Staph. aureus. Knowledge of the biotypes of Staph. intermedius has remained virtually unchanged since the description of the species by Hajek (1976) and Staph. hyicus has remained largely unexplored, though more recently some advances have been made (Takeuchi et al. 1987). Interesting observations on differing populations of several other staphylococcal species have been made by Kloos and co-workers and considered in a wider perspective by Kloos (1980).

Most, but not all, biotypes described by Hajek & MarSalek (1971), as well as by other authors, can be designated as ecovars of Staph. aureus, Staph. intermedius or Staph. hyicus because they are associated with distinct ecosystems, in this instance, different animal hosts. The term ecovar is most appro- priate and meaningful here. As discussed by Kloos (1980), such subpopulations may be good candidates for subspecies ranking but only when they are distinguishable by phenotypic characters as well as by small, but significant differences in DNA-DNA homology values or other genomic mea- surements.

The use of many different modifications and extensions of the Hajek and MarSalek scheme for staphylococcal biotyping has complicated the picture. The situation with regard to Staph. aureus can be summarized as follows. Generally only one human ecovar (biotype A) is recognized, though some strains, especially those of phage group 11, are considered to be a somewhat special group (Galinsky 1975). Staphylokinase production is the most characteristic trait of the human ecovar. Poultry strains form a very homogeneous group which differs from most swine strains, with which they were placed in one biotype (biotype B) by Hajek and MarSalek (1971), by the absence of /?-haemolysin production. In some countries, however, most swine strains are also p-haemolysin-negative and cannot therefore be differentiated from poultry Staph. aureus by this trait (Shimizu et al. 1987). Strains belonging to the bovine and ovine ecovar (biotype C) coagulate bovine plasma rapidly but bovine

Staphylococci in animals 75s biotype strains differ from ovine strains in their growth type on crystal violet agar. Strains from hares are usually non-pigmented and also form a distinct ecovar (biotype D). Shimizu et al. (1986) described one further ecovar-biotype G+omposed mainly of staphylokinase-positive strains isolated from rodents which rapidly coagulated bovine plasma. Such strains also occur frequently on horses (Devriese et al. 1984b).

Usually many, but not all, and sometimes not even the majority of Staph. aureus strains isolated from a given animal host, can be allotted to well-defined ecovars. Considerable variations occur depending on the host species (Hummel et al. 1982a). Live chickens carry, almost exclusively, a well defined poultry ecovar and this situation has remained unchanged for the last 20 years despite the changes in poultry keeping that have occurred during this period. However, strains which can be recognized as clearly belonging to the bovine ecovar account for only a minority of Staph. aureus isolated from bovine mastitis (Hummel et a / . 1982a; Devriese 1984).

Staphylococcus aureus ecovars can be distinguished by biochemical characters such as staphylokinase (fibrinolysin of the older literature), haemolysins (especially /I-haemolysin), coagulation of bovine plasma and growth type on agar media containing crystal violet. Other biochemical characteristics have been used to distinguish Staph. intermedius biotypes (Hajek 1976). Typing with specialized phages has proved to be useful mainly in studies with Staph. aureus strains from poultry (Gibbs et al. 1978b; Shimizu 1977) and sheep (Oeding et al. 1976). Specialized phage typing sets have been devel- oped to type Staph. intermedius (Blouse & Meekins 1968) and Staph. hyicus (Kawano et al. 1983). Other means of typing that show promise in the distinction of biotypes among animal strains, have apparently not been widely used to date. They include proteolytic zymograms which distinguished between Staph. hyicus from pigs, chickens or cows (Takeuchi et al. 1987); esterase patterns which are useful in the differentiation of Staph. intermeditis biotypes (Schleifer et a/ . 1976); coagulase typing (Kawano et al. 1986); bacteriocin typing (Skalka 1986), and analysis of bacteriolytic activity patterns (Varaldo et al. 1978).

Depending on the scope of the work a simple or a more thorough approach to the biotyping of strains of Staph. aureus can be used. It should be noted, however, that most of the tests used in biotyping are fraught with difficulties. Even the simplest may yield erratic results without careful standardization (Devriese 1984). When it is of interest to determine only whether or not a particular strain or a series of strains belongs to human or animal ec0vars-e.g. to determine a source of infection-it may be sufficient to test for staphylokinase or protein A production. Since its discovery in 1935 by Madison, staphylokinase production has been shown by many authors to be a typical characteristic of human Staph. aureus strains. About 6&75% of human strains and, in the case of lesion strains, even higher proportions (Hinton & Orr 1957) produce this enzyme and among strains of animal origin its presence suggests a human origin. Only in horses and rodents does the kinase- positive biotype G of Shimizu et al. (1986) (see above) complicate the situation. It should be noted, however, that staphylokinase production is an unstable character in certain strains, which can change y lysogenic conversion (Winkler et al. 1965). This is probably not a frequent event in uiuo. In many cases the commercially available protein A test offers a useful alternative to the staphylokinase tests. Protein A is usually present in human Staph. aureus, less frequently in bovine strains and rarely or not at all in staphylococci of other biotypes (Oeding 1983; Akay et al. 1985).

5. Transfer to unusual hosts and zoonotic aspects

Animal ecovars of Staph. aureus do not readily colonize or infect humans. In a detailed study of nasal colonization of workers on dairy and pig farms, Hummel et al. (1978) and Hummel & Witte (1981) found that typical animal ecovars colonized humans only rarely. Strains which could not be assigned to known ecovars and which differed only in certain traits, such as staphylokinase or j?-haemolysin were, however, not infrequently isolated from the milkers as well as from the udders.

No well-documented cases of Staph. aureus infections in man caused by animal strains have appeared in the literature. One recent report describes the isolation of Staph. intermedius from wounds caused by dog bites (Talan et a/ . 1989) but it is not clear what role these staphylococci played in the infections. The reverse situation, infection or colonization of animals with human Staph. aureus,

76s L. A . Devriese appears to be much more frequent. Although precise data are not available, many observations indicate that Staphylococcus aureus from human sources do not cause dangerous infections in animals. This is illustrated by the following examples. Methicillin-resistant Staph. aureus, which are of much importance in the human hospital environment, were demonstrated in cases of cattle mastitis on some farms in the early seventies (Devriese & Hommez 1975). They disappeared spontaneously despite the increase in the use of penicillinase-stable penicillins and cephalosporins in the prevention and treatment of staphylococcal mastitis in cows. The strains showed the biotype characteristics typical of the human methicillin-resistant strains and similar phage-sensitivities. It should be noted, however, that human strains of Staph. aureus have been implicated as the cause of sizable outbreaks of udder infection in cattle (Hummel & Meene 1979).

It has often been reported that Staph. aureus occurs in dogs and in the 1960s infections with phage type 80/81 strains, which were much feared in human hospitals at that time, were described. In our experience, however, Staph. aureus strains occur in dogs mostly as secondary invaders in infections caused by Staph. intermedius or they may be found, together with a mixed flora, in eczematous lesions of atopic patients. Biberstein et al. (1984) reported that canine skin infections (particularly pyoderma, long known to involve coagulase-positive staphylococci as the only significant bacterial component) were associated in their practice almost exclusively with Staph. intermedius, while 10 to 15% of staphylococci from other canine sources were Staph. aureus. In cats Staph. aureus, usually belonging to the human biotype (Devriese et al. 1984a), and Staph. intermedius strains are probably not primary pathogens. Their significance is difficult to assess.

The course and the severity of Staph. aureus infections in rabbits caused by human ecovar strains were compared by Okerman et al. (1984) with those caused by a rabbit ecovar, the characteristics of which were very similar to the hare Staph. aureus biotype as described by Hajek & Margalek (1971). Under identical conditions losses due to the hare/rabbit ecovar were much more severe. The human strains caused only sporadic lesions whereas the hare/rabbit ecovar caused a protracted epidemic of mastitis in the does and exudative dermatitis in their young.

Food intoxication caused by staphylococcal enterotoxins in foods of animal origin poses a special case of possible carry over of disease agents from animals to man. While there is general agreement on the frequent production of enterotoxins by human strains of Staph. aureus, findings with animal strains, except those from sheep, are very heterogenous and often apparently contradictory. Hajek 8t MarHalek (1973) used the cellophane-over-agar and gel precipitation technique and found only 1% of enterotoxin producers in a large collection of animal Staph. aureus and Staph. interrnedius strains belonging to five different biotypes. Not less than 61% of human ecovar strains from cases of bronchopneumonia were positive in similar tests. On the other hand, Olsvik et al. (1981), who used an ELISA procedure, detected 50% positive animal and 31% positive human strains. However, only two of their 55 positive strains from animals produced more than 1 pg/ml enterotoxin in the growth conditions used, but this amount or more was produced by five of the 15 human strains tested under similar conditions. Apparently contradictory results have also been published with poultry strains. Shiozowa et al. (1980) found that only 2.7% were enterotoxin-producers, but Harvey et al. (1982) detected high percentages of enterotoxin D-producers among poultry strains of a well-defined phage susceptibility group. It should be noted that the carcass flora after plucking may be largely composed of strains which are endemic to slaughterhouses and which have replaced the staphylococcal flora of the live birds (Notermans et al. 1982; Adams 8t Mead 1983; Dodd et al. 1988).

Results obtained with Staph. aureus strains from sheep milk have been more uniform. These strains often produce enterotoxin C (Hajek 1978; GuitiCrrez et al. 1982). The situation is less clear with bovine strains. Takeshige et al. (1983) reported frequent production of enterotoxin C, but most of the positive strains also produced staphylokinase, a characteristic of the human ecovar. Niskanen 8t Koiranen (1977) and Olsvik et al. (1981) also found many strains which produced enterotoxin C, often in combination with B. Goat strains belonging to the ovine ecovar frequently produce enterotoxin C, but they also produce the toxic shock syndrome toxin 1 (de Centorbi et al. 1988).

It can be concluded that, in general, animal Staph. aureus strains are less likely to cause food poisoning than are those of human origin. Enterotoxin C, the most frequent enterotoxin of animal Staph. aureus ecovars, is less heat-stable than enterotoxin A and B and also less toxic for men

Staphylococci in animals 77s (Casman 1965; Bergdoll 1970). However, changes in staphylococcal populations and replacement of strains of live animals by human or slaughterhouse-associated ecovars during slaughtering and food processing can be important, as is discussed elsewhere (see Mead & Dodd: this Symposium pp. 81s-91s). A somewhat unexpected finding in this context is the frequent production of enterotoxin A, the most important cause of staphylococcal food intoxication, by Staph. interrnedius strains from dogs (Fukuda et al. 1984).

With thz possible exception of mink (Juokslahti et al. 1980), staphylococcal enterotoxicosis does not occur, or has remained undiagnosed, in animals. This is remarkable because animals such as monkeys, cats and dogs have been used in the experimental reproduction of the disease, albeit usually by intravenous or intraperitoneal inoculation. Certain mammalian species are susceptible to oral administration. This has been shown with enterotoxin A in pigs (Taylor e t a/. 1982) and mink (Juokslahti et a/. 1980).

6. Conclusions

The observations on the distribution of species and ecovars on different hosts and body sites as well as the zoonotic aspects of staphylococcal disease and enterotoxicosis reviewed above, illustrate how biotyping has been and can be used to trace the origins of certain infections and to assess the importance of animal contacts. They also indicate highly specialized and successful host-parasite relation- ships, the underlying mechanisms of which are unknown. The elucidation of these-represents a most interesting challenge. With the staphylococci we are still far away from explanations such as those of the 'key and lock' type that have been demonstrated so convincingly to form the basis of adhesion and colonization by certain Gram-negative bacteria.

The study of different staphylococcal species which possess or lack those properties associated with pathogenicity in Staph. aureus, offers a useful approach for the assessment of the importance of different pathogenicity factors.

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Staphylococci in healthy and diseased animals