Equine salmonellosis

M G COLLETT AND T D MOGG

GENERAL INTRODUCTION: FACULTATIVELY ANAEROBIC GRAM-NEGATIVE RODS Salmonella spp. infections

Introduction

Salmonellosis is an important infectious disease of horses of all ages, usually caused by non-host-specific salmonellas (especially Salmonella Typhimurium). The disease occurs in most countries and is diagnosed sporadically. Depending on the age group, the disease manifests as peracute septicaemia, acute enterotyphlocolitis, chronic diarrhoea, failure to thrive or, more rarely, polyarthritis, orchitis, fistulous withers or abortion. Salmonellosis may affect individual horses or, at times, it occurs in extensive epidemics in groups of horses that are at risk. Outbreaks in foals on stud farms have been reported in several countries.^{7, 9, 45, 87} Foals and aged, debilitated or stressed horses are particularly susceptible.^{27, 87} Asymptomatic carriers play an important role in the epidemiology of the disease. Nosocomial Salmonella infections are common in large equine clinics or hospitals.^{21, 49} Severe outbreaks in such institutions may force their temporary closure in order to control the disease.⁸

More than a century ago, the most common manifestation of equine salmonellosis was abortion due to the hostspecific Salmonella Abortusequi.^{6, 27} Since then the prevalence of abortion has declined markedly to the extent that isolations of S. Abortusequi in the USA virtually ceased by the 1970s.^{49, 50} Abortion is still a problem in India,^{26, 72} where other Salmonella serovars are also implicated in the syndrome,⁴² as well as in Croatia,⁴⁴ Italy¹⁷ and Argentina.²⁵ Although Henning in 1956³¹ reported S. Abortusequi as the cause of purulent tendovaginitis, bursitis and pneumonia in horses in South Africa, it has not been isolated in the country since 1970.³²

Aetiology

For the general morphological and physicochemical properties of the salmonellas, consult the introduction, Salmonella spp. infections.

At least 40 of the known serovars of Salmonella have been isolated from horses. Several serovars may occur in contaminated environments at the same time, and the simultaneous infection of an animal with two or even more serovars is not uncommon. When this does occur, it is usually reason for a poor prognosis.^{50, 68}

Apart from S. Typhimurium, other serovars isolated from cases of equid salmonellosis include S. Enteritidis, S. Anatum, S. Newport, S. Heidelberg, S. Typhimurium var. Copenhagen, S. Kottbus, S. Dublin, S. Saint-paul, S. Hadar, S. Ohio, S. Agona, and S. Krefeld.^{7, 8, 22, 27, 50, 67, 77} Some investigators regard S. Typhimurium and S. Typhimurium var. Copenhagen to be the most pathogenic,⁸ while others believe that S. Anatum infection has the gravest prognosis.⁵⁰ Numerous phage types of S. Typhimurium have been shown to be involved in equine infections. However, in most cases no clear conclusions can be reached regarding the origin of the various types, even of phage types known to originate from wild birds, such as finches, sparrows and pigeons.^{7, 27} It appears that the susceptibility of horses when exposed to sufficient numbers of salmonellas — irrespective of sero- or phage type — is similar to that in other animal species.²⁷

Epidemiology

The prevalence of salmonellosis in horses on stud farms has been reported to range from 0,36 to 27 per cent. It has been estimated that up to 10 per cent of horses in the USA may be infected with the organism at some time or another.⁵⁰ In a recent study in the USA the prevalence of faecal shedding of a Salmonella serovar in normal horses was 0,8 per cent: isolates from faeces were from eight serogroups and represented 14 serotypes, the most common being S. Muenchen.⁸¹

Horses most frequently become infected via the oral route, although infection may also take place through the mucous membranes of the eyes and the nose via aerosol droplets.⁷⁵ Experimental infection of horses can be achieved with oral doses ranging from 9,5 × 10⁶ to 8,8 × 10¹¹ organisms.⁶⁸

There are many environmental sources of infection, but particular problems are posed by contamination of water by effluent, contaminated feed (meat or bone meal and milk products) and dietary additives, as well as carrier birds, rodents, horses and other farm animal species that excrete the bacteria.^{27, 87}

In a recent study in the USA, the prevalence of salmonellas in grain and other concentrates used for horse feed was 0,4 per cent. Isolates from feed represented three serotypes, none of which were also identified in the faeces of shedding horses.⁸¹ An infected foal can excrete 3 × 10⁵ organisms per gram of faeces, resulting in significant environmental contamination.⁵⁰

In a population of horses, up to 24 per cent may be asymptomatic carriers, based on faecal cultures.^{67, 76, 81} In one Australian study, 1,65 per cent of the normal non-hospitalized horse population were found to be shedding salmonellas in their faeces, while 23,8 per cent of horses hospitalized in a veterinary teaching hospital were shedders.⁶⁷ The prevalence of asymptomatic carriers in healthy adult horses, as assessed by culture of mesenteric lymph nodes at a slaughter facility, was 71,4 per cent.⁴⁷ On the other hand, another study based on the culture of mesenteric lymph nodes from horses submitted for necropsy at a veterinary teaching hospital found a Salmonella prevalence of only 1,96 per cent.³⁸ On studs experiencing outbreaks of salmonellosis in foals, up to 30 per cent of clinically normal foals may have salmonellas in their faeces.⁹ The bacterium can be harboured by carrier animals in the mesenteric lymph nodes, liver, spleen and/or ileum.^{46, 50}

Asymptomatic carrier horses may or may not actively shed salmonellas in their faeces.^{9, 50, 84} Shedders appear to play a major role in the dissemination of the organisms.⁵⁰ It appears that stress can activate the infection in carrier animals, and it may not only enhance the faecal excretion of Salmonella organisms but also sometimes precipitate overt clinical disease. Faecal excretion is intermittent, and while the numbers of salmonellas excreted are usually low, the quantities are sufficient to contaminate the environment to a threatening extent, particularly in areas of close confinement such as veterinary hospitals.⁵ True persistently infected carriers, such as occurs with host-adapted salmonellas (e.g. S. Dublin in cattle), probably rarely occur in horses.⁷⁷

Most horses recovering from clinical salmonellosis shed salmonellas in their faeces for less than 30 days; however, some may shed for up to 300 days.^{7, 77} Various serovars of Salmonella may be isolated from carriers but, in keeping with the prevalence of specific serovars, S. Typhimurium is most commonly isolated from both asymptomatic carriers and horses with clinical disease.^{5, 8, 49} Two or even three serovars may, however, be isolated from an animal at any specific time.⁵⁰

On horse stud farms where salmonellosis is endemic, salmonellas may frequently be isolated from soil samples from areas of high-density stocking, such as around water troughs, under trees, near gateways and in foaling paddocks.⁹ Salmonellas can survive in shaded soils for nine months or more.⁹ Where horses are kept on properties that had previously been stocked with sheep and/or cattle, faecal contamination from these animals may be a source of infection for horses.⁹ Outbreaks most frequently occur during summer and autumn, when the ambient temperature is highest.⁸ This may reflect the optimal conditions for growth of the organism and susceptibility of the host.^{37, 77}

Salmonellosis in horses is rarely a simple cause-and-effect phenomenon, and the appearance of overt disease is generally regarded as being a sequel to one or more predisposing factors²⁷ including debility, stress (such as that induced by long periods of transport, a new environment, new stable-mates, hot humid weather, dietary changes, unfamiliar handlers, general anaesthesia, surgery, excessive work, overtraining and intercurrent disease) and anthelmintic or antimicrobial therapy.^{27, 50, 57} It appears that the changes in gut flora that occur during stress or antimicrobial (especially oxytetracycline) therapy allow salmonellas to multiply.^{37, 56, 57, 75} Colic, abdominal surgery and the oral administration of antimicrobials appear to be important risk factors for the induction of Salmonella infections.^{34, 64} The chances of isolating salmonellas from horses are about ten times greater in those that are receiving antimicrobial therapy than in those that are not. In addition, combined oral and parenteral antimicrobial treatment increases by 40-fold the chance of a horse contracting salmonellosis.³⁴ The probability of salmonellas being isolated from horses suffering from colic is two to five times higher than it is from those that are presented with other medical complaints.^{34, 35, 59} Salmonellas were isolated from 55,3 per cent of those horses that had faecal cultures performed because they had developed diarrhoea after surgery for colic.¹⁴ Horses suffering from small colon impactions, especially those treated surgically, were found to be at increased risk for salmonellosis.⁶⁶

The close confinement of large numbers of horses with a variety of medical and surgical problems in hospitals or clinics creates an ideal situation for the development of outbreaks of nosocomial salmonellosis.³⁵ Such disease may result from infection of hospitalized horses by an ‘in-house’ organism,³⁶ or by the introduction into the hospital population of an organism by an asymptomatic carrier or animal with frank salmonellosis.⁷⁶ Asymptomatic carriers may be shedding the bacteria on admission to the hospital or be induced to shed (and potentially develop overt disease) by one of the predisposing factors listed above. Several studies have attempted to identify risk factors associated with the faecal shedding of salmonellas in hospitalized horses and the development of nosocomial infections.^{35, 36, 40, 82} Risk factors identified in one or more of these studies have included high ambient temperature, dietary changes, development of diarrhoea before or soon after admission, development of fever, development of leukopenia, impactions of the large colon, and nasogastric intubation. Nosocomial infections can result in significant morbidity in patients admitted to the hospital for reasons other than salmonellosis (e.g. elective surgery, and non-enteric medical disorders) and in many outbreaks the result is death or euthanasia for humane reasons of many patients.

Financial losses associated with hospital closures and containment of the infection can be substantial.⁴⁰ Several detailed descriptions of such outbreaks have recently been published.^{29, 71, 80}

The epidemiology of the diseases caused by S. Abortusequi is poorly understood. The bacterium occurs exclusively in equids, including donkeys, and causes abortion, genital infections, orchitis and arthritis.^{72, 83} It does not occur in the intestinal tract and has not been isolated from faeces. The role played by stallions in the dissemination of the organisms is unknown, but venereal transmission does appear to be a distinct possibility.⁷² Salmonella Abortusequi is disseminated on stud farms by direct or indirect contact with the products of abortion that contain large numbers of organisms. A high prevalence of abortion generally occurs only in the first foaling season after the infection has been introduced. Thereafter abortion is restricted to new arrivals. Infected mares may produce live foals but most of them die shortly after birth.⁷⁰

Pathogenesis

The pathogenesis of salmonellosis in horses has been poorly studied but it is probably similar to that in other domestic species (see Bovine salmonellosis and Ovine and caprine salmonellosis).

Stress and other factors mentioned above play significant roles in the initiation, course and outcome of the disease.⁵⁰ Pathogenic salmonellas invade the mucosa of the intestinal tract, where they are phagocytosed by macrophages and neutrophils. Salmonellas can survive within macrophages and thus escape injury by the host immune system and many antimicrobials.⁷⁷ Bacterial virulence factors and the inflammatory response by the host against the infection appear to contribute to the development of the disease.⁵⁴

Clinical signs

The clinical signs of enteric or septicaemic salmonellosis in horses are similar to those occurring in the comparable disease in other species.

Animals may manifest clinical signs and clinicopathologic responses within 24 to 72 hours of oral exposure to salmonellas,^{58, 68} stressful events⁵⁷ or other predisposing factors. In experimentally induced equine salmonellosis, an elevated body temperature is accompanied by a severe neutropenia during the first five days. This is followed by a rebound neutrophilia.⁵⁸ The peak of pyrexia generally precedes the onset of diarrhoea by one or two days.⁶⁸ Animals suffering from diarrhoea may exhibit a decrease in plasma proteins, and marked electrolyte and acid-base abnormalities.^{11, 37, 68}

In general, three overlapping clinical forms of salmonellosis occur. The most severe is a peracute, fatal septicaemic disease, most often affecting foals one to six months of age. Affected foals show fever, weakness, depression, lethargy and reduced appetite. Visible mucous membranes may appear ‘muddy’ and petechiated.⁸⁷ Signs of enteritis may be absent or there may be increased borborygmus and a severe, foetid diarrhoea containing mucus.⁸⁷ The diarrhoea may have a characteristic green colour and may contain blood.⁴ If untreated, affected animals usually die within 24 to 72 hours. Complications of septicaemic salmonellosis include acute, purulent meningitis, arthritis in one or more joints, physitis and osteomyelitis.^{28, 37, 79, 88} Culture of Salmonella from septic arthritis in foals is a significant indicator of a poor prognosis for survival.⁷⁸ On affected studs, the annual foal mortality rate as a result of septicaemic salmonellosis may range from 4 to 20 per cent.⁹

The acute disease, which is the commonest form, is characterized initially by pyrexia, loss of appetite, a severe enterotyphlocolitis (typified by profuse green or brown watery faeces containing mucus, blood and shreds of intestinal mucosa), tachycardia and dehydration. Mild colic may precede the onset of diarrhoea.⁸⁸ The course of the disease may extend over a period of several weeks. The fever and diarrhoea may become intermittent as the disease progresses. The severity and duration of diarrhoea depend on the infecting Salmonella serovar and host immunity.⁸⁸ With appropriate therapy these animals usually survive, despite dehydration and rapid weight loss. Septicaemia may lead to organ localization (e.g. joints and/or bone), especially in foals. Complications of enterocolitis such as endotoxic shock, laminitis, thrombophlebitis, coagulopathies, acute renal failure and chronic malabsorption may result in increased morbidity and death. In some cases euthanasia may need to be performed for humane reasons.¹¹

The chronic form, which is the rarest, has a duration of three weeks to several months and is characterized by the passing of loose, soft faeces, intermittent fever, poor appetite, significant weight loss and dehydration.²⁷ Animals suffering from this form of the disease but with a shorter course often recover, while those that remain ill for more extended periods usually die after being terminally recumbent as a result of severe weakness.⁵⁰ Proof of the aetiological involvement of salmonellas in this form is often contentious.⁸⁸

Other manifestations of salmonellosis in horses have been reported. Adult horses may only manifest fever, anorexia and severe depression in the absence of any other clinical signs.⁷³ Mild infections may manifest only as colic without diarrhoea.⁸⁸ Colic of varying severity may be accompanied by diarrhoea, or adynamic ileus and persistent gastric reflux (proximal enteritis).⁸⁸

Pregnant mares infected with S. Abortusequi usually abort during the latter half of gestation.^{70, 72} The incubation period is about 30 days.⁷⁰ There are often no indications of impending abortion.⁴⁴ Following abortion the foetal membranes may be retained and there may be a copious vaginal discharge.⁴⁴

Pathology

Lesions in animals that have died of the disease vary according to the syndrome from which they had suffered.

In the peracute or acute septicaemic disease, petechial and ecchymotic haemorrhages are present especially in serosal membranes (particularly the pericardium and peritoneum) and along the course of visceral blood vessels.⁷ Petechiae may be present in the heart valves, bladder mucosa, and renal and adrenal cortices. The renal cortices are generally pale in contrast to the medullary congestion which is often present.⁴ The spleen is enlarged and the lungs are congested and oedematous.⁴ The gastric mucosa is intensely hyperaemic, with some scattered haemorrhages and oedema. There may be congestion and catarrhal inflammation of the small intestine and the visceral lymph nodes are enlarged, oedematous, and may be haemorrhagic.

In animals that have died from the acute enterotyphlocolitis syndrome, lesions are usually present in the mucosa of the entire caecum, which is severely hyperaemic, and proximal large colon, and occasionally in the distal ileum. The lesions are those of a severe acute fibrinonecrotic in- flammatory process, often with small ulcers and occasionally multiple small abscesses in the gut wall.^{4, 7, 37, 68} Affected parts of the gut wall may be oedematous. The contents of the large intestine are watery and foul-smelling. Histologically, affected parts of the intestine reveal varying degrees of superficial mucosal necrosis, lymphocyte and neutrophil infiltration into the lamina propria, thrombosis of proprial capillaries, lymphoid depletion in Peyer’s patches, and the presence of occasional bacterial colonies.^{4, 68, 87} The necrotic mucosa may be covered by a fibrinocellular pseudomembrane.⁴ The germinal centres in mesenteric lymph nodes may also be depleted and bacterial colonies may be evident within sinuses.⁸⁷ There may be macroscopic or microscopic evidence of localization of the infection in other sites, with the development of lesions such as suppurative meningitis, cerebral abscessation, suppurative arthritis, and epiphyseal or metaphyseal osteomyelitis.^{7, 28, 63}

Lesions in chronic salmonellosis are not nearly as marked as they are in the acute disease;⁴ a patchy fibrinous or ulcerative colitis or typhlitis may be present, and residual fibrotic intestinal adhesions may contribute to death following colic or adynamic ileus.^{4, 7}

Foetuses that have been aborted as a result of S. Abortusequi infections are well formed with no anatomic abnormalities, and show relatively mild, non-specific gross pathological changes such as subcutaneous oedema, petechial haemorrhages and lung oedema. The placentas from aborted mares that have aborted show striking lesions. Scattered chocolate-brown necrotic foci are surrounded by areas of erythema and oedema and occasional haemor rhages. Histologically, the placental lesions include oedema, haemorrhage, prominent suppuration and masses of Gram-negative rod-shaped bacteria.⁴⁴ Salmonella Abortusequi may also cause arthritis in foals and orchitis in stallions.⁷² The orchitis may be suppurative with abscess formation.⁴³

Diagnosis

Salmonellosis may be suspected on the basis of history, physical examination findings and supporting clinicopathologic data. For example, the rapid development of a marked neutropenia is a frequent portend of acute enteric salmonellosis.²¹ Because of the non-specific clinical signs of the disease, the diagnosis should be confirmed by isolation of salmonellas from affected horses. Serological tests are of limited value in the establishment of a diagnosis, as most horses contain antibodies to salmonellas and because a rise in titre is not always marked during the course of the disease.⁵⁸A definitive diagnosis, determination of the origin of the causative bacteria, and control may require a detailed investigation including the serotyping, biotyping and phage-typing of the organism, application of biochemical and antibiotic sensitivity tests, and perusal of hospital case records.⁵

In order to diagnose enteric salmonellosis antemortem it is essential that serial faecal cultures be performed, as the isolation of Salmonella from infected animals, even during the course of clinical disease, is inconsistent.⁷³ Multiple faecal cultures are superior to single culture attempts.⁸⁴ Rectal mucosal biopsy (a safe and rapid technique) is more sensitive (52 per cent) than faecal culture (32 per cent) in detecting salmonellas.⁶⁰ When the two are used in combination the success rate may rise to 60 per cent.⁵⁹ In order to enhance the laboratory detection of salmonellas, samples consisting of 20 to 50 g faeces are preferable to rectal swabs. Antimicrobial therapy does not eliminate salmonellas from the faeces of infected horses (i.e. salmonellas can still be cultured), even when isolates are sensitive to the antimicrobial being administered.^{49, 84}

Salmonellas survive in the refrigerator for two to four weeks.⁸⁸ The use of selective and enrichment media, including tetrathionate or selenite broth, and brilliant green or Salmonella-Shigella agar increase the likelihood of positive culture.^{51, 84}Pre-enrichment with buffered peptone water may improve the sensitivity of culture media for salmonellas.⁸⁶ Possible reasons for the difficulties in isolating salmonellas from carrier animals are that the organisms are shed intermittently or that they may be sublethally ‘damaged’ by the host immune system, necessitating culturing in an enrichment medium to ‘revive’ the organism.⁸⁴ Horses suffering from subclinical infections excrete low numbers of organisms (as low as 10 CFU/g faeces) compared to horses with clinical salmonellosis (up to 10⁵ CFU/g).⁷⁷

Methods for the detection of salmonellas in faeces using the polymerase chain reaction (PCR) have been developed.^{1, 16}

These methods are more sensitive, more rapid and require the submission of fewer samples than for microbiologic culture.¹⁵ Both viable bacteria and nonviable DNA can be detected by application of PCR tests. While a positive PCR test on faeces confirms that the horse is shedding salmonellas (viable or nonviable), the signifi- cance of PCR-positive but culture-negative horses with respect to environmental contamination is unclear.¹

In live animals with the septicaemic form, blood and/or appropriate samples from localized sites of infection (e.g. joint or bone), if present, can be cultured for salmonellas. The results of blood culture are, however, frequently disappointing.⁶⁸

Salmonella serovars are readily cultured from specimens of the intestinal tract and the internal organs collected at necropsy from animals that have died of the septicaemic form of the disease.^{37, 87} Necropsy specimens for bacteriological examination should always include mesenteric and ileocolonic lymph nodes and sections of the wall of the caecum and proximal large colon, liver and spleen in separate containers.^{68, 74, 87} In cases of enteric salmonellosis, cultures made from tissues obtained after the death of the animal may be positive, even when antemortem faecal cultures were repeatedly negative.¹¹

Serology is unlikely to be a reliable indicator of infection or immune status.⁶⁸

In cases of abortion due to S. Abortusequi infection, the organism can be isolated from tissues of the aborted foetus, such as heart blood, internal organs, stomach and intestinal contents, and from the foetal membranes, as well as from swabs of the vaginal exudate of the mare.⁷²

Differential diagnosis

Depending on the syndrome, several diseases may be confused with salmonellosis.

In young foals suffering from the septicaemic form, a number of other bacterial diseases, particularly those caused by Escherichia coli, Actinobacillus equuli, Klebsiella spp., and beta-haemolytic streptococci, should be considered.⁶³

In the enteric form of salmonellosis in foals, conditions such as nutritional diarrhoea, infections with rotavirus, certain strains of E. coli, Clostridium perfringens, Clostridium difficile, Rhodococcus equi, Cryptosporidium spp. or Giardia spp., and helminth-related diarrhoeas should be considered as differential diagnoses.^{55, 89, 90} Concurrent infections (e.g. with rotavirus) may occur.²³ In older animals suffering from acute enteric salmonellosis, differential diagnoses include endotoxic shock, C. perfringens type A or C. difficile infections, acute peritonitis and typhlocolitis due to Ehrlichia risticii infection (see Potomac horse fever).^{20, 88}

In horses with colic due to salmonellosis, other causes of abdominal pain need to be differentiated. Differential diagnoses for horses suffering from persistent gastric reflux in clude other infectious causes of proximal enteritis (e.g. C. perfringens) ⁸⁸ and small intestinal obstructive lesions.

The administration of certain antimicrobials, notably oxytetracycline,^{3, 18} lincomycin,⁶⁵ and less commonly tylosin, penicillins, cephalosporins, potentiated sulphonamides and erythromycin¹² may precipitate acute colitis. Excessive dosages of non-steroidal anti-inflammatory drugs have also been associated with diarrhoea in horses.⁵² Chronic salmonellosis should be differentiated from strongyle larval migrans, cyathostomosis, granulomatous enteritis, alimentary lymphosarcoma, chronic R. equi infection, sand enteropathy, chronic liver disease, food allergies and fermentative disorders.^{13, 48}

Apart from salmonellas, common causes of infectious arthritis and osteomyelitis (‘joint ill’) in young foals — often with evidence of systemic illness — are E. coli, Klebsiella spp., beta-haemolytic streptococci, A. equuli and R. equi. ^{28, 61}

Control

All horses suspected to be infected with Salmonella, should be regarded as positive for the organism and appropriate isolation measures instituted until such time as multiple faecal cultures (using enrichment techniques) are negative.⁸⁴ Salmonellosis is a zoonotic disease and suitable precautions to avoid human infections should be applied.⁷⁴ Young children, the eldery and immunocompromised people are most at risk.⁷⁷

Supportive therapies, with the emphasis on intravenous fluid replacement, correction of electrolyte deficiencies and acid-base abnormalities, and good nursing are paramount in the treatment of salmonellosis.^{11, 27, 49, 68} Successful treatment of acute enterocolitis is dependent on the ability to administer appropriate fluid therapy. Oral fluid replacement may increase the severity of the diarrhoea.²⁷ Antidiarrhoeal drugs such as bismuth subsalicylate or activated charcoal may be used, but these should be discontinued after three days if they have not produced a beneficial effect. Non-steroidal anti-inflammatory drugs, such as low doses of flunixin meglumine, may be used for their anti-endotoxic effects. Other therapies aimed at ameliorating the effects of endotoxaemia (e.g. plasma containing antibodies to Gramnegative core antigens, polymixin B, pentoxifylline) may also be considered.^{41, 75} Plasma transfusions may help to alleviate the hypoproteinaemia which develops as a consequence of the enteropathy.¹¹

Antimicrobial therapy for the treatment of enteric salmonellosis in adult horses is of questionable value and does not necessarily resultin the elimination of salmonellas from the intestinal tract. Organisms may still be isolated from the faeces and tissues during and after the completion of the course of treatment.^{7, 49, 50} Antimicrobial therapy is more effective when initiated prior to the development of diarrhoea, or when it is used to control systemic or septicaemic Salmonella infections.²⁷ It should be kept in mind that once diarrhoea has developed, oral antimicrobial treatment (particularly with oxytetracycline), may aggravate the severity of the diarrhoea.²⁷

Foals with either the enteric or septicaemic forms of the disease should be treated with aggressive parenteral antimicrobial therapy due to the high mortality associated with these forms and the predisposition for localization of the infection. Parenteral antimicrobial therapy should also be considered for adult horses with enteric salmonellosis that have in dwelling intravenous catheters or that are neutropenic. Multi-drug resistant salmonellas have been isolated from horses in both the northern and southern hemispheres.^{2, 10, 19, 30, 39, 85} Antimicrobial therapy should thus be based on local sensitivity patterns. Since salmonellas can survive intracellularly, lipid soluble antimicrobials are preferred.⁷⁷

Horses may succumb to the disease despite appropriate and aggressive antimicrobial therapy.^{5, 50} Animals may also survive the chronic disease but subsequently fail to reach their previous level of performance.⁴⁹

During an outbreak, affected animals should be physically isolated and their faeces and bedding burnt.²⁷ Attendants should be acquainted with the dangers of spreading the infection and instructed in proper hygienic procedures (e.g. protective boots and clothing and the use of disinfectant footbaths). The faeces of all other horses (and other ‘incontact’ animals, e.g. pets) on the property should be cultured for Salmonella on numerous occasions and positive animals should be isolated. Bedding, feed, water and other environmental samples should be cultured for Salmonella. Sources of environmental contamination (e.g. sewage) need to be identified.⁷⁴ Other precautions for containing the infection should include the prevention of the contamination of the feed and water of all the horses in the establishment, and the control of flies and rodents.²⁷

An animal which has been infected with salmonellas should not be returned to its farm of origin, or allowed to mix with uninfected animals, until five consecutive specimens of its faeces have proved to be negative for salmonellas. It has been suggested that daily faecal cultures for three to four weeks may be necessary to be reasonably certain that an animal is not shedding the bacterium.⁷⁵

Suitable disinfection of veterinary equipment, tack and the environment should be performed following treatment of horses with salmonellosis. In a recent study, bleach (5,25 per cent sodium hypochlorite diluted 1:32) was the most effective disinfectant on a range of common surfaces.²⁴ Environmental cultures or PCR tests should be used to confirm successful disinfection, and can also be used to identify locations harbouring the organism. Where there is heavy soil and environmental contamination, spraying with 5 per cent formalin at monthly intervals has been shown to effectively kill salmonellas.⁶⁹

To reduce the possibility of salmonellosis developing in horses admitted to veterinary hospitals, every effort must be made to minimize stress. Horses with normal haemograms should have surgery within the first 48 hours of admission to the hospital, or, if the haemogram is not within normal limits, surgery should be delayed for at least a week. Animals should be sent home as soon as possible after surgery.²¹ Protocols designed to attempt to prevent the development of nosocomial infections include strict isolation of horses admitted with diarrhoea or that develop diarrhoea following admission, rapid isolation of horses that develop clinical or clinicopathologic signs (e.g. fever, neutropenia) of salmonellosis, routine faecal cultures or PCR tests of patient populations deemed to be at risk (e.g. intensive care patients), altering traffic patterns to minimize contact between patients, routine handwashing between patients, wearing protective clothing (e.g. plastic boots and/or gloves) to minimize cross contamination, cessation of sharing equipment (e.g. thermometers, nasogastric tubes) between patients, stringent stall cleaning and disinfection, and control of rodents and birds within the hospital.^{29, 53, 71, 80} Commercial probiotic preparations failed to decrease the incidence of faecal Salmonella shedding, or diarrhoea, in horses admitted to a veterinary teaching hospital for colic surgery.⁶² Containment of nosocomial infections often requires aggressive disinfection procedures and/or closure of part or all of the hospital.^{29, 71, 80}

The extensive use of formalin-killed bacterins has been reported in a number of countries, but controlled studies have not been undertaken to determine their efficacy.^{5, 7, 33} When a vaccine is used, it is imperative that the serovars prevailing in the outbreakin question bemonitored against those presentin the vaccine in order to determine whether or not its use is warranted. In order that colostrum-derived passive immunity can be provided in foals, pregnant mares should be vaccinated at least 30 days prior to foaling, while foals should be vaccinated at two to three months of age to effect control of the condition.^{7, 9, 33} A commercial vaccine (Fort Dodge Australia) containing washed cells of S. Typhimurium is available for the control of foal salmonellosis. Preliminary studies on the development of an S. Abortusequi vaccine for the control of outbreaks of abortion have shown that experimentally a betapropriolactone-inactivated chrome alum vaccine provides better protection in mice than a formalin-inactivated vaccine.⁸³ When required, autogenous vaccines can be prepared for use in specific outbreaks.^{9, 75}

Management practices should lessen exposure of horses to possible sources of infection and also minimize stressful situations that may precipitate the disease.⁷⁴ Prudent use of antimicrobial agents in horses is warranted to avoid antimicrobial-associated salmonellosis.

References

1. AMAVISIT, P., BROWNING, G.F., LIGHTFOOT, D., CHURCH, S., ANDERSON, G.A., WHITHEAR, K.G. & MARKAM, P.F., 2001. Rapid PCR detection of Salmonella in horse faecal samples. Veterinary Microbiology, 79, 63–74.
2. AMAVISIT, P., MARKAM, P.F., LIGHTFOOT, D., WHITHEAR, K.G. & BROWNING, G.F., 2001. Molecular epidemiology of Salmonella Heidelberg in an equine hospital. Veterinary Microbiology, 80, 85–98.
3. ANDERSSON, G., EKMAN, L., MANSSON, I., PERSSON, S., RUBARTH, S. & TUFVESSON, G., 1971. Lethal complications following administration of oxytetracycline in the horse. Nordisk Veterinaer Medicin, 23, 9–22.
4. BARKER, I.K., VAN DREUMEL, A.A. & PALMER, N., 1993. The alimentary system. In: JUBB, K.V.F., KENNEDY, P.C. & PALMER, N., (eds). Pathology of Domestic Animals, Vol. II, 4th edn. San Diego: Academic Press, Inc.
5. BEGG, A.P., JOHNSTONE, K.G., HUTCHINS, D.R. & EDWARDS, D.J., 1988. Some aspects of the epidemiology of equine salmonellosis. Australian Veterinary Journal, 65, 221–223
6. BRUNER, D.W. & MORAN, A.B., 1949. Salmonella infections of domestic animals. Cornell Veterinarian, 39, 53–63.
7. BRYANS, J.T., FALLON, E.H. & SHEPHARD, B.P., 1961. Equine salmonellosis. Cornell Veterinarian, 51, 467–477.
8. CARTER, J.D., HIRD, D.W., FARVER, T.B. & HJERPE, C.A., 1986. Salmonellosis in hospitalized horses: Seasonality and case fatality rates. Journal of the American Veterinary Medical Association, 188, 163–167.
9. CARTER, M.E., DEWES, H.G. & GRIFFITHS, O.V., 1979. Salmonellosis in foals. Journal of Equine Medicine and Surgery, 3, 78–83.
10. CASTOR, M.L., WOOLEY, R.E., SHOTTS, E.B., BROWN, J. & PAYEUR, J.B., 1989. Characteristics of Salmonella isolated from an outbreak of equine salmonellosis in a veterinary teaching hospital. Journal of Equine Veterinary Science, 9, 236–241.
11. COHEN, N.D., 1999. Salmonellosis. In: COLAHAN, P.T., MERRITT, A.M., MOORE, J.N. & MAYHEW, I.G., (eds). Equine Medicine and Surgery, 5th edn. St. Louis: Mosby. pp. 749–753.
12. COHEN, N.D., 1999. Antibiotic-associated diarrhea. In: colahan, p.t., merritt, a.m., moore, j.n. & mayhew, i.g., (eds). Equine Medicine and Surgery, 5th edn. St. Louis: Mosby. pp. 763–764
13. COHEN, N.D., 1999. Chronic diarrhea. In: COLAHAN, P.T., MERRITT, A.M., MOORE, J.N. & MAYHEW, I.G., (eds). Equine Medicine and Surgery, 5th edn. St. Louis: Mosby. pp. 764–767.
14. COHEN, N.D. & HONNAS, C.M., 1996. Risk factors associated with development of diarrhoea in horses after celiotomy for colic: 190 cases (1990–1994). Journal of the American Veterinary Medical Association, 209, 810–813.
15. COHEN, N.D., MARTIN, L.J., SIMPSON, R.B., WALLIS, D.E. & NEIBERGS, H.L., 1996. Comparison of polymerase chain reaction and microbiological culture for detection of salmonellas in equine feces and environmental samples. American Journal of Veterinary Research, 57, 780–786.
16. COHEN, N.D., NEIBERGS, H.L., WALLIS, D.E., SIMPSON, R.B., MCGRUDER, E.D. & HARGIS, B.M., 1994. Genus-specific detection of salmonellas in equine feces by the use of the polymerase chain reaction. American Journal of Veterinary Research, 55, 1049–1054.
17. CONDOLEO, R., ROPERTO,F., AMADDEO, D., GUARINO, G., FONTANELLI, G & TRONCONE, A., 1983. Abortion and perinatal mortality in horses. Microbiological, virological and histopathological observations. Acta Medica Veterinaria, 29, 469–480.
18. COOK, W.R., 1973. Diarrhoea in the horse associated with stress and tetracycline therapy. The Veterinary Record, 93, 15–16.
19. DONAHUE, J.M., 1986. Emergence of antibiotic-resistant Salmonella agona in horses in Kentucky. Journal of the American Veterinary Medical Association, 188, 592–594.
20. DONALDSON, M.T. & PALMER. J.E., 1999. Prevalence of Clostridium perfringens enterotoxin and Clostridium difficile toxin A in feces of horses with diarrhea and colic. Journal of the American Veterinary Medical Association, 215, 358–361.
21. DORN, C.R., COFFMAN, J.R., SCHMIDT, D.A., GARNER, H.E., ADDISON, J.B. & MCCUNE, E.L., 1975. Neutropenia and salmonellosis in hospitalized horses. Journal of the American Veterinary Medical Association, 166, 65–67.
22. DOYLE, A.W. & BAKER, W., 1971. Salmonella dublin infection in a thoroughbred foal. Irish Veterinary Journal, 25, 141–143.
23. EUGSTER, A.K., WHITFORD, H.W. & MEHR, L.E., 1978. Concurrent rotavirus and Salmonella infections in foals. Journal of the American Veterinary Medical Association, 173, 857–858.
24. EWART, S.L., SCHOTT, H.C., ROBISON, R.L., DWYER, R.M., EBERHART, S.W. & WALKER, R.D., 2001. Identification of sources of Salmonella organisms in a veterinary teaching hospital and evaluation of the effects of disinfectants on detection of Salmonella organisms on surface materials. Journal of the American Veterinary Medical Association, 218, 1145–1151.
25. FUMUSO, E., SOTO, P., JACA, D., SPARO, M., ARACIL, E. & BELLUSCI, J., 1997. Outbreak of abortion in mares due to Salmonella abortusequi. Revista de Medicina Veterinaria (Buenos Aires), 78, 86–88.
26. GARG, D.N. & MANCHANDA, V.P., 1986. Prevalence and aetiology of equine abortion. Indian Journal of Animal Sciences, 56, 730–735.
27. GIBBONS, D.F., 1980. Equine salmonellosis: A review. The Veterinary Record, 106, 356–359.
28. GOEDEGEBUURE, S.A., DIK, K.J., FIRTH, E.C. & MERKENS, H.W., 1980. Polyarthritis and polyosteomyelitis in foals. Veterinary Pathology, 17, 651.
29. HARTMANN, F.A., CALLAN, R.J., MCGUIRK, S.M. & WEST, S.E.H., 1996. Control of an outbreak of salmonellosis caused by drug-resistant Salmonella anatum in horses at a veterinary hospital and measures to prevent future infections. Journal of the American Veterinary Medical Association, 209, 629–631.
30. HARTMANN, F.A. & WEST, S.E.H., 1995. Antimicrobial susceptibility profiles of multidrug-resistant Salmonella anatum isolated from horses. Journal of Veterinary Diagnostic Investigation, 7, 159–161.
31. HENNING, M.W., 1956. Animal Diseases in South Africa. 3rd edn. Pretoria: Central New Agency
32. HENTON, M.M., 2001. Onderstepoort Veterinary Institute. Personal communication.
33. HIBBS, C.M. & COFFMAN, J.R., 1967. Immunologic response of the equine to Salmonella typhimurium bacterin. Cornell Veterinarian, 57, 454–464.
34. HIRD, D.W., CASEBOLT, D.B., CARTER, J.D., PAPPAIOANOU, M. & HJERPE, C.A., 1986. Risk factors for salmonellosis in hospitalized horses. Journal of the American Veterinary Medical Association, 188, 173–177.
35. HIRD, D.W., PAPPAIOANOU, M. & SMITH, B.P., 1984. Case-control study of risk factors associated with isolation of Salmonella saint-paul in hospitalized horses. American Journal of Epidemiology, 120, 852–864
36. HOUSE, J.K., MAINAR-JAIME, R.C., SMITH, B.P., HOUSE, A, & KAMIYA, D.Y., 1999. Risk factors for nosocomial Salmonella infection among hospitalized horses. Journal of the American Veterinary Medical Association, 214, 1511–1516.
37. HOUSE, J.K. & SMITH, B.P., 2000. Salmonella in horses. In: WRAY, C. & WRAY, A., (eds.). Salmonella in Domestic Animals. Cabi Publishing, Oxon, UK, pp. 219–230.
38. HOUSE, J.K., SMITH, B.P., WILDMAN, T.R., CARRIGAN, M.J. & KAMIYA, D.Y., 1999. Isolation of Salmonella organisms from the mesenteric lymph nodes of horses at necropsy. Journal of the American Veterinary Medical Association, 215, 507–510.
39. IKEDA, J.S. & HIRSH, D.C., 1985. Common plasmid encoding resistance to ampicillin, chloramphenicol, gentamicin and trimethoprimsulfadiazine in two serotypes of Salmonella isolated during an outbreak of equine salmonellosis. American Journal of Veterinary Research, 46, 769–773
40. KIM, L., MORLEY, P.S., TRAUB-DARGATZ, J.L., SALMAN, M.D. & GENTRY-WEEKS, C., 2001. Factors associated with Salmonella shedding among equine colic patients at a veterinary teaching hospital. Journal of the American Veterinary Medical Association, 218, 740–748.
41. KOHN, C.W., 1999. Medical therapy for gastrointestinal diseases. In: COLAHAN, P.T., MERRITT, A.M., MOORE, J.N. & MAYHEW, I.G., (eds). Equine Medicine and Surgery, 5th edn. St. Louis: Mosby. pp. 603–620.
42. KUMAR, S. & GUPTA, B.K., 1972. Salmonella anatum from an aborted foal. British Veterinary Journal, 128, lxiv.
43. LADDS, P.W., 1993. The male genital system. In: JUBB, K.V.F., KENNEDY, P.C. & PALMER, N., (eds). Pathology of Domestic Animals, Vol. III, 4th edn. San Diego: Academic Press, Inc.
44. MADIC, J., HAJSIG, D., SOSTARIC, B., CURIC, S., SEOL, B., NAGLIC, T. & CVETNIC, Z., 1997. An outbreak of abortion in mares associated with Salmonella abortusequi infection. Equine Veterinary Journal, 29, 230–233.
45. MAHAFFEY, L.W., 1952. Salmonella typhimurium in foals in Western Australia. Australian Veterinary Journal, 28, 8.
46. MANN, P.H., CAVRINI, C. & PIERACCI, F., 1964. Salmonella organisms found in healthy horses at slaughter. Cornell Veterinarian, 54, 495–500.
47. MCCAIN, C.S. & POWELL, J.K., 1990. Asymptomatic salmonellosis in healthy horses. Journal of Veterinary Diagnostic Investigation, 2, 236–237.
48. MERRITT, A.M., BOLTON, J.R. & CIMPRICH, R., 1975. Differential diagnosis of diarrhoea in horses over six months of age. Journal of the South African Veterinary Association, 46, 73–76.
49. MORSE, E.V., DUNCAN, M.A., FESSLER, J.F. & PAGE, E.H., 1976. The treatment of salmonellosis in equidae. Modern Veterinary Practice, 57, 47–51.
50. MORSE, E.V., DUNCAN, M.A., PAGE, E.A. & FESSLER, J.F., 1976. Salmonellosis in equidae: A study of 23 cases. Cornell Veterinarian, 66, 198–213.
51. MURRAY, M.J., 1989. Diarrhea. In: BROWN, C.M., (ed.). Problems in Equine Medicine. Philadelphia: Lea & Febiger
52. MURRAY, M.J., 1997. Acute colitis. In: ROBINSON, N.E., (ed.). Current Therapy in Equine Medicine 4. Philadelphia: W.B. Saunders Company. pp. 197–203.
53. MURRAY, M.J., 1996. Salmonellosis in horses. Journal of the American Veterinary Medical Association, 209, 558–560.
54. MURRAY, M.J., DORAN, R.E., PFEIFFER, C.J., TYLER, D.E., MOORE, J.N. & SRIRANGANATHAN, N., 1989. Comparative effects of cholera toxin, Salmonella typhimurium culture lysate, and viable Salmonella typhimurium in isolated colon segments in ponies. American Journal of Veterinary Research, 50, 22–28.
55. NETHERWOOD, T., WOOD, J.L.N., TOWNSEND, H.G.G., MUMFORD, J.A. & CHANTER, N., 1996. Foal diarrhoea between 1991 and 1994 in the United Kingdom associated with Clostridium perfringens, rotavirus, Strongyloides westeri and Cryptosporidium spp. Epidemiology and Infection, 117, 375–383.
56. OWEN, R. AP R., 1975. Post-stress diarrhoea in the horse. The Veterinary Record, 96, 267–270.
57. OWEN, R. AP R., FULLERTON, J. & BARNUM, D.A., 1983. Effects of transportation, surgery, and antibiotic therapy in ponies infected with Salmonella. American Journal of Veterinary Research, 44, 46–50.
58. OWEN, R. AP R., FULLERTON, J.N., TIZARD, I.R., LUMSDEN, J.H. & BARNUM, D.A., 1979. Studies on experimental enteric salmonellosis in ponies. Canadian Journal of Comparative Medicine, 43, 247–254.
59. PALMER, J.E., BENSON, C.E. & WHITLOCK, R.H., 1985. Salmonella shed by horses with colic. Journal of the American Veterinary Medical Association, 187, 256–257.
60. PALMER, J.E., WHITLOCK, R.H., BENSON, C.E., BECHT, J.L., MORRIS, D.D. & ACLAND, H.M., 1985. Comparison of rectal mucosal cultures and fecal cultures in detecting Salmonella infection in horses and cattle. American Journal of Veterinary Research, 46, 697–698.
61. PALMER, N., 1993. Bones and joints.In: JUBB, K.V.F., KENNEDY, P.C. & PALMER, N., (eds). Pathology of Domestic Animals, Vol I, 4th edn. San Diego: Academic Press, Inc.
62. PARRAGA, M.E., SPIER, S.J., THURMOND, M. & HIRSH, D., 1997. A clinical trial of probiotic administration for prevention of Salmonella shedding in the postoperative period in horses with colic. Journal of Veterinary Internal Medicine, 11, 36–41.
63. PLATT, H., 1973. Septicaemia in the foal. A review of 61 cases. British Veterinary Journal, 129, 221–229.
64. PUOTUNEN-REINERT, A. & HUSKAMP, B., 1986. Acute postoperative diarrhoea in colic horses. Journal of the South African Veterinary Association, 57, 5–11.
65. RAISBECK, M.F., HOLT, G.R. & OSWEILER, G.D., 1981. Lincomycin associated colitis in horses. Journal of the American Veterinary Medical Association, 179, 362–363.
66. RHOADS, W.S., BARTON, M.H. & PARKS, A.H., 1999. Comparison of medical and surgical treatment for impaction of the small colon in horses: 84 cases (1986–1996). Journal of the American Veterinary Medical Association, 214, 1042–1047.
67. ROBERTS, M.C. & O’BOYLE, D.A., 1981. The prevalence and epizootiology of salmonellosis among horses in South Eastern Queensland. Australian Veterinary Journal, 57, 27–35
68. ROBERTS, M.C. & O’BOYLE, D.A., 1982. Experimental Salmonella anatum infection in horses. Australian Veterinary Journal, 58, 232–240.
69. ROBINSON, R.A., SHORTRIDGE, E.H. & MACDIARMID, H.J., 1970. The effects of monthly formalin treatments on the survival of salmonellas in earthen sheep yard debris. New Zealand Veterinary Journal, 18, 214–216.
70. SCHAETZ, F., 1984. Diseases of the female genital organs and reproductive disorders. In: DIETZ, O. & WIESNER, E., (eds). Diseases of the Horse. A Handbook for Science and Practice, Part 2/1, p. 362. Basel: S. Karger.
71. SCHOTT, H.C., EWART, S.L., WALKER, R.D., DWYER, R.M., DIETRICH, S., EBERHART, S.W., KUSEY, J., STICK, J.A. & DERKSEN, F.J., 2001. An outbreak of salmonellosis among horses at a veterinary teaching hospital. Journal of the American Veterinary Medical Association, 218, 1152–1159.
72. SINGH, I.P., SHARMA, V.K. & KAURA, Y.K., 1971. Some aspects of the epidemiology of Salmonella abortus-equi infection in equines. British Veterinary Journal, 127, 378–383
73. SMITH, B.P., 1979. Atypical salmonellosis in horses: Fever and depression without diarrhea. Journal of the American Veterinary Medical Association, 175, 69–71.
74. SMITH, B.P., 1981. Equine salmonellosis: A contemporary view. Equine Veterinary Journal, 13, 147–151.
75. SMITH, B.P., 1990. Salmonellosis: Paranoia or reason to worry? Compendium on Continuing Education for the Practising Veterinarian, 10, 1459–1461.
76. SMITH, B.P., RIENA-GUERRA, M. & HARDY, A.J., 1978. Prevalence and epizootiology of equine salmonellosis. Journal of the American Veterinary Medical Association, 172, 353–356.
77. SPIER, S.J., 1993. Salmonellosis. Veterinary Clinics of North America: Equine Practice, 9, 385–397
78. STEEL, C.M., HUNT, A.R., ADAMS, P.L.E., ROBERTSON, I.D. CHICKEN, C., YOVICH, J.A. & STICK, J.A., 1999. Factors associated with prognosis for survival and athletic use in foals with septic arthritis: 93 cases (1987– 1994). Journal of the American Veterinary Medical Association, 215, 973–977.
79. STUART, B.P., MARTIN, B.R., WILLIAMS, L.P. & VON BYERN, H., 1973. Salmonella-induced meningoencephalitis in a foal. Journal of the American Veterinary Medical Association, 162, 211–213
80. TILLOTSON, K., SAVAGE, C.J., SALMAN, M.D., GENTRY-WEEKS, C.R., RICE, D., FEDORKA-CRAY, P.J., HENDRICKSON, D.A., JONES, R.L., NELSON, W. & TRAUB-DARGATZ, J.L., 1997. Outbreak of Salmonella infantis infection in a large animal veterinary teaching hospital. Journal of the American Veterinary Medical Association, 211, 1554–1557.
81. TRAUB-DARGATZ, J.L., GARBER, L.P., FEDORKA-CRAY, P.J., LADELY, S. & FERRIS, K.E., 2000. Fecal shedding of Salmonella spp. by horses in the United States during 1998 and 1999 and detection of Salmonella spp. in grain and concentrate sources on equine operations. Journal of the American Veterinary Medical Association, 217, 226–230.
82. TRAUB-DARGATZ, J.L., SALMAN, M.D. & JONES, R.J., 1990. Epidemiologic study of salmonellas shedding in the feces of horses and potential risk factors for the development of infection in hospitalized horses. Journal of the American Veterinary Medical Association, 196, 1617–1622.
83. UPPAL, P.K. & KATARIA, J.M., 1987. Epidemic of Salmonella abortus equi abortion in horses and some studies on the development of a vaccine. Journal of Reproduction and Fertility Supplement, No. 35, 669–670.
84. VAN DUIJKEREN, E., FLEMMING, C., SLOET VAN OLDRUITENBORGHOOSTERBAAN, M., KALSBEEK, H.C. & VAN DER GIESSEN, J.W.B., 1995. Diagnosing salmonellosis in horses — culturing of multiple versus single faecal samples. The Veterinary Quarterly, 17, 63–66.
85. VAN DUIJKEREN, E., SLOET VAN OLDRUITENBORGH-OOSTERBAAN, M., HOUWERS, D.J., VAN LEEUWEN, W.J. & KALSBEEK., H.C., 1994. Equine salmonellosis in a Dutch veterinary teaching hospital. The Veterinary Record, 135, 248–250.
86. WALTMAN, W.D., 2000. Methods for the cultural isolation of Salmonella. In: WRAY, C. & WRAY, A., (eds). Salmonella in Domestic Animals. Oxon, UK: CABI Publishing. pp. 355–372.
87. WENKOFF, M.S., 1973. Salmonella typhimurium septicemia in foals. Canadian Veterinary Journal, 14, 284–287.
88. WHITLOCK, R.H., 1986. Colitis: Differential diagnosis and treatment. Equine Veterinary Journal, 18, 278–283.
89. WILSON, J.H. & CUDD, T.A., 1990. Common digestive tract problems: diarrhoea. In. KOTERBA, A.M., DRUMMOND, W.H. & KOSCH, P.C., (eds). Equine Clinical Neonatology. Baltimore: Williams & Wilkins. pp. 424–430.
90. XIAO, L. & HERD, R.P., 1994. Epidemiology of equine Cryptosporidium and Giardia infections. Equine Veterinary Journal, 26, 14–17