Bovine salmonellosis

S G FENWICK AND M G COLLETT

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

Introduction

Bovine salmonellosis usually manifests clinically as a syndrome of septicaemia, acute or chronic enteritis, or abortion. One or more of these syndromes may occur simultaneously in the same animal or herd. Calves less than three months of age are most commonly affected, while animals exposed to stressful situations are particularly prone to contract the disease. Although salmonellosis in cattle is caused by a number of different serovars, Salmonella Dublin and S. Typhimurium are by far the most common. The source of infection is usually an environment contaminated by the faeces of either clinically affected or carrier animals. Carrier animals play an important role in the epidemiology of Salmonella infections. Salmonellosis is a zoonosis.

A disease of calves that was subsequently considered to be salmonellosis was first diagnosed in South Africa by Hutcheon in 1893.⁴⁸ It was similar to the condition described by O. Henning in 1894 as ‘lewerziekte’ (liver disease) or ‘yellow liver’.⁴⁸ Salmonella Dublin as a cause of abortion in cattle in South Africa was first reported in 1943.¹⁰

Salmonellosis in both calves and adult cattle occurs in most countries of the world and has been shown to be economically important in Europe and North America.^{61, 102, 150} In any outbreak, the economic impact will depend on the rates of morbidity and mortality.⁹⁷ In South Africa, the disease is frequently diagnosed in calves, but it is only rarely encountered as a clinical problem in adult cattle.^{48, 122} Although an accurate estimate of the occurrence of salmonellosis in southern Africa is not available, its importance (especially in calves) is likely to be similar to that in many other parts of the world.⁵⁶

Aetiology

Serovars of the genus Salmonella are identified on the basis of specific combinations of somatic and flagellar antigens and, to a lesser extent, by their biochemical reactions (see the introduction to Salmonella spp. infections).

Salmonella Dublin and S. Typhimurium are the serovars most frequently associated with bovine salmonellosis;^{49, 83, 102} other serovars (e.g. S. Newport, S. Bovismorbificans) are incriminated only rarely.^{5, 17, 150} Henning in 1939⁴⁷ and 1953⁴⁸ reported that more than 95 per cent of cases of salmonellosis in calves in South Africa were due to S. Dublin, while Botes in 1965¹¹ recorded that S. Typhimurium infection was responsible for up to 19,1 per cent of cases. Recently in New Zealand, S. Brandenburg has been reported increasingly as a cause of enteritis and abortions.²⁰

In the UK, epidemics due to S. Typhimurium phage types DT104, DT193 and DT204C, which are resistant to a range of antibacterials (such as chloramphenicol), have emerged since 1977.^{55, 128, 152} The phage type DT104 possesses in vitro resistance to ampicillin, chloramphenicol, streptomycin, sulphonamides and tetracycline (R-type ACSSuT), as well as apramycin,⁷⁶ and has also been detected in France⁶ and the USA.^{8, 9} Of even more concern is the increasing emergence of trimethoprim and fluoroquinolone resistance in phage type DT104,^{25, 130} and that resistant clones can spread rapidly.¹

For information on the general characteristics of the salmonellas, consult the introduction to Salmonella spp. infections.

Epidemiology

The diseases in cattle caused by S. Dublin and S. Typhimurium are clinically indistinguishable, but they differ epidemiologically (Table 151.1).^{2, 112, 151} The host preferences¹⁴⁵ and the ability of the two serovars to establish carriers in animals following initial infection also differ.^{2, 13, 16, 46, 105, 145, 151, 156}

Salmonella Dublin is regarded as a serovar specific to cattle and only rarely infects other species of animals and humans.^{13, 116, 141}On the other hand,most other serovars, including S. Typhimurium, are not host-specific,¹⁵⁶ and direct or indirect transmission of S. Typhimurium between cattle as well as from other domestic (e.g. sheep) or wild animals to cattle, and vice versa, may occur.^{13, 110, 156}

Table 151.1 Important epidemiological differences between Salmonella Dublin and Salmonella Typhimurium infections in cattle

SALMONELLA DUBLIN	SALMONELLA TYPHIMURIUM
Bovine-specific145	Not host-specific156
Usually endemic herd problem151	Usually sporadic disease outbreaks: Calf-rearing units60, 122, 151
Bovine carriers important as source of infection13, 105	Various animal species and their products are important sources of infection81, 105, 158
Carriers excrete organisms for long periods (sometimes life-long)145	Carriers excrete organisms for short periods (usually three to four months)105, 145
Septicaemia common2	Septicaemia uncommon: enteritis more common2
Abortions relatively common52, 54, 151	Abortions uncommon145, 151

Calves aged between 2 and 12 weeks are the most frequent victims of salmonellosis, but mature cattle may also suffer from clinical disease.^{2, 3, 11, 49, 105, 110, 145} In calves infected with S. Dublin, salmonellosis usually occurs at between 6 and 12 weeks of age, whereas disease caused by S. Typhimurium is most common in the first three weeks of life.^{11, 158} The possible explanation for this difference is that S. Dublin infection is more prevalent in adult cattle than S. Typhimurium;¹⁵⁶ consequently, the presence of colostral immunity to S. Dublin is more common in calves than immunity to S. Typhimurium.¹⁵⁸ The disease is much more common in dairy than in beef calves, mainly because of differences in management practices.¹³ In contrast to the general husbandry practices applied to beef calves, dairy calves are usually removed from their mothers at a very early age and many of them are then subjected to the stresses of transportation, starvation, changes in environment and feed, and mixing with calves from different farms. These factors all predispose them to salmonellosis.^{4, 46, 110, 160}

In outbreaks of bovine salmonellosis, the morbidity rate may reach 50 per cent while the case fatality rate in untreated animals can reach 100 per cent.¹⁰²

Managemental, physiological and nutritional factors, as well as intercurrent infections,^{145, 156} not only predispose animals to salmonellosis, but may also precipitate clinical disease in infected cattle and the excretion of the bacteria by carrier animals.^{82, 105, 145} Predisposing factors for calves include unhygienic conditions,^{110, 160} overcrowding, transportation,^{46, 82} insufficient intake of colostrum, inadequate availability of water and food¹⁸ and inclement weather. Hospitalization, surgery, overcrowding, parturition and sudden dietary changes can predispose adult cattle to Salmonella infection.^{17, 54, 66, 122} Intercurrent infections which may play a role include bovine viral diarrhoea (BVD) and infectious bovine rhinotracheitis viruses and Escherichia coli, or infestations with parasites such as Fasciola hepatica. ^{96, 127, 145, 151} In a series of experiments, clinical signs tended to be more severe in dual infections with BVD and Salmonella than with Salmonella alone, suggesting that BVD exacerbates the effects of Salmonella infection.¹⁵⁵ The effects of these ‘stress factors’ are probably related to the suppression of cell-mediated immunity.⁷

The most important sources of salmonellas are clinically affected and carrier animals, and faecally contaminated environments, water and feedstuffs (e.g. bone, fish and soya-bean meals).^{41, 106, 144, 156} Clinically affected animals excrete large numbers of bacteria, particularly in their faeces. Scouring calves have been shown to excrete up to 10⁸ organisms per gram of faeces within 24 hours of infection, rising to 10¹⁰ per gram after that.²⁸ Apart from faecal excretion, organisms may also be excreted in the urine¹³ and the saliva (originating from the tonsils or salivary glands) of diseased calves,^{3, 107, 145} as well as in the milk of cows in which salmonellas have colonized the udder.^{39, 89, 115, 141, 145, 148} Salmonellas can survive in colostrum stored at 5 to 11 °C for more than 30 days.¹⁵³ Adult cattle are important in the dissemination of salmonellas as they act as carriers, particularly of S. Dublin.^{105, 146, 151} Salmonella Dublin may be excreted in the milk, faeces and urine of cows for up to four weeks after parturition or abortion.^{13, 54} Persistent excretion of S. Typhimurium DT104 in milk has been recorded in a dairy herd in the UK.¹¹⁵ Excretion of S. Newport for 11 months after a disease outbreak has also been documented.¹⁰⁶ Clinically normal calves can occasionally act as carriers.^{55, 72} Carrier animals harbour organisms in their mesenteric lymph nodes, gut-associated lymphoid tissue, macrophages in the lamina propria of the intestine, ruminal fluid, and the gall bladder.^{7, 36, 112, 113} Stressed animals have greater numbers of organisms and shed them more readily and in higher numbers than non-stressed carriers.^{26, 36, 82}Calves in rearing units are frequently infected following the introduction of clinically normal carrier animals from other properties or saleyards.¹⁵⁶

Animals that graze with active carriers (animals that are faecal excreters of the organism)may ingest and shed salmonellas in their faeces and are referred to as ‘passive carriers’, as they stop excreting the bacteria when they are removed from the source of infection.^{13, 105} Active carriers may excrete 10³ to 10⁵ organisms per gram of faeces.¹¹⁹ Carriers that do not excrete salmonellas in their faeces are referred to as ‘latent carriers’.¹⁰²

Cattle carrying S. Dublin may either lose the infection or remain life-long carriers,^{105, 150} shedding organisms intermittently or continuously in large numbers in their faeces.^{40, 105, 112, 119, 145} Parturition is probably an important event in the activation of latent carriers of S. Dublin and this can lead to congenital infection of calves.¹⁰³ The administration of dexamethasone to carrier animals can precipitate clinical signs, even to the extent of septicaemia, and increased shedding of salmonellas.¹²⁰ In contrast, cattle carrying S. Typhimurium generally shed the bacteria for a limited period only, in most instances no longer than three to four months.^{105, 145} Salmonellosis in calves can be self-limiting in two to five weeks.^{28, 55} In addition to cattle, a wide range of other domestic and wild animals, particularly rodents and birds, may also be carriers of S. Typhimurium and shed the organism into the environment.^{45, 47, 85, 144} Rodents may also be reservoirs of S. Dublin.¹²³

In Botswana 7 per cent of cattle have been reported to be carriers of Salmonella infections, but the overall situation in southern Africa is unknown.⁸³ Prevalence rates of carriers from a number of non-southern African countries have ranged from 5 to 15 per cent in dairy cattle, and a rate of 4 per cent has been recorded in beef cattle.¹⁰² However, these estimates are likely to be low because cattle may excrete organisms intermittently, and stress could precipitate excretion by latent carriers.¹⁴⁵

Apart from carrier or diseased animals, other sources of Salmonella include animal feedstuffs whose constituents may be infected prior to formulation or become contaminated thereafter,^{4, 12, 105, 144} poultry manure and litter (which are commonly used as a feed supplement for cattle in southern Africa because of their high nitrogen content),¹⁴⁵ and water contaminated by sewage.^{22, 145} The practice of using effluent to irrigate pastures may disseminate the infection widely and expose large numbers of cattle to salmonellosis.^{63, 145} Infections may be related to the level of contamination; calves grazing pasture to which 10⁶ S. Dublin per millilitre of slurry had been applied the previous day became infected, whereas no clinical cases were seen when pastures had an application of slurry containing only 10³ organisms per millilitre.¹²⁶ The risk of infection in calves grazing pastures contaminated with slurry is considered to be low.¹²⁵ Water sources, particularly in the vicinity of informal settlements with unsatisfactory sewage disposal facilities, may become contaminated with salmonellas and can also widely disseminate the bacteria.^{22, 23, 144, 145} The use of communal calf milk substitute dispensers (e.g. ‘calfetaria’) can play a role in the spread of infection.¹¹⁰ The feeding of unpasteurized milk or milk from bulk tanks with contaminated milk-line filters can also be sources of infection for calves.^{23, 39, 72, 80, 110}

Veterinarians may aid in the dissemination of infection between farms.¹⁴⁷ Salmonellas have been isolated from gumboots worn on infected properties, even after scrubbing in warm water and a quaternary ammonium disinfectant. The organisms can also be transmitted on the wheels of vehicles.¹⁷

Contamination of market premises and transport vehicles has been shown to play a role in the epidemiology of Salmonella infection in calves.¹⁵⁹ Concern has been expressed as to the possibility of nosocomial infections and the spread of salmonellas in veterinary teaching hospitals due to the movement of staff, students, clients and visitors.⁶²

Salmonella organisms may survive in the environment for variable periods when suitable conditions ofmoisture and organic material are present.^{109, 126, 144, 156} For example, S. Dublin has been found to survive for ten months to six years in faeces splashed on stall surfaces^{38, 98} and for over one year in the environment under a wide range of climatic conditions.^{81, 104} Salmonella Typhimurium, on the other hand, has been reported to persist in contaminated rearing premises, pastures and soil for between four months and two years.^{81, 117, 134, 145} Salmonella Typhimurium has been shown to survive in urine for up to five days.⁹⁸ Salmonella Montevideo was recovered from multiple sites on a California dairy two years after a clinical outbreak of salmonellosis.³⁷

Most Salmonella infections occur by the faecal-oral route.^{45, 90, 92, 157} Aerosol transmission has been reported but is rare.^{45, 100, 139} Conjunctival infection of calves has been achieved experimentally.²⁸ Calves may occasionally become infected transplacentally.^{27, 105} Intensive farming units with close contact between calves favour the transmission of salmonellas.^{3, 4, 145}

The minimum oral dose of various serovars required to induce clinical enteric disease varies from 10⁴ to 10¹¹ organisms^{7, 28, 86, 114, 118, 142, 149, 156, 157} with the oral route requiring about 25 per cent more bacteria than respiratory infection.¹⁰⁰ The larger the challenge dose, the higher the morbidity and mortality rates, especially in younger calves; survival is inversely related to the size of the challenge inoculum.^{114, 118} Clearly, therefore, the larger the number of organisms in the environment, the more likely it is that a susceptible animal will contract salmonellosis.¹¹⁹ The intravenous inoculation of 10⁸ or more S. Dublin organisms is capable of inducing abortion in pregnant heifers.⁴² Inoculation of 5 × 10³ colony forming units of S. Dublin into the teat canal can induce persistently infected carrier animals.¹²⁰

Salmonellosis is a zoonosis, S. Typhimurium being more commonly involved than S. Dublin.^{13, 46} The organisms can readily be transmitted from animals to humans by ingestion or inhalation.^{4, 16, 29, 46, 137, 156} Animal-derived food, especially raw milk, meat and eggs, is the most important source of infection for people.^{4, 148} The high fat content of milk protects the organisms from the acidic environment of the stomach, allowing them to pass through it unscathed.¹³ As an example of the potential impact of zoonotic infection, a single dairy cow in Canada shed S. Enteritidis in milk continuously for seven months and was responsible for a number of infections in people ingesting the raw milk from the bulk tank.¹⁴⁸ Although the transmission of infection by direct contact between humans is uncommon, outbreaks can occur in hospitals and in family groups.⁴

People working with animals are at risk of contracting the disease (e.g. from carrier calves or adults),⁷² while the risk is even greater when treating clinically affected animals.^{16, 138} In this regard, a number of farmers and veterinarians in New Zealand have contracted S. Brandenburg infections through contact with aborted foetuses and infected cows and ewes.³² Cutaneous infections of veterinary surgeons handling aborting animals is recognized as an occupational hazard.^{137, 147} In contrast, humans who are excretors of Salmonella organisms can provide a source of infection for animals.^{4, 85, 145} For example, calves may become infected when they are taught to drink milk from a bucket by attendants who are themselves infected.¹⁴⁵

Pathogenesis

Salmonellas are facultative intracellular organisms and survive in macrophage phagolysosomes where they are protected from the effects of antibody and complement.¹⁰² This is particularly important in latent carriers where the effects of stress (e.g. parturition) can induce the active shedding of organisms.¹⁰² The outcome of infection with Salmonella depends essentially on three factors: the size of infective dose, predisposing factors influencing the host, and the level of immunity.^{7, 109, 145}

A feature of serovars more commonly associated with systemic infections, e.g. S. Dublin, is the presence of plasmid-encoded spv genes which promote enhanced intracellular proliferation in intestinal tissues and at extra-intestinal sites in the natural host. The spv genes are found in nearly all natural isolates of Salmonella that are host-adapted to animals, but only a proportion of broad-host-range serovars carry the genes.⁷⁵

In bovine salmonellosis, only the intestinal tract may be involved or, if the organisms manage to spread beyond the intestinal mucosa and mesenteric lymph nodes, septicaemia or bacteraemia may develop and result in dissemination particularly to the liver, tonsils, spleen, lungs and lymph nodes. A second bacteraemia can follow with localization of salmonellas at sites such as the joints, meninges and placenta, especially the cotyledons.^{7, 43, 69, 109, 114, 142} One or more active nutrients, present in placentomes, may promote the growth of salmonellas.¹⁵⁴ In this regard, erythritol, a factor responsible for the localization of Brucella abortus in the bovine uterus, has been eliminated.⁵³ Pregnant animals may abort without evidence of enteric disease.⁶⁰ Foetal death is due to septicaemia and/or placentitis.⁵² Since premature live infected calves can result, abortion in late pregnancy is probably not stimulated by foetal death; rather, hormonal changes resulting from the placentitis may be responsible.⁴³ In closed herds, the primary clinical manifestation (such as pneumonia, abortion, enteritis or polyarthritis) of S. Dublin infections may differ from year to year.¹²³

The pathogenesis of the enteric lesions has two stages;colonization and invasion of the intestine by the bacteria, followed by increased secretion of fluid and electrolytes.^{7, 87}

Colonization and invasion of the intestine

Salmonellas must be ingested in sufficient numbers (generally a minimal infective dose of at least 10⁴ organisms is required) for colonization of the distal small intestine and colon to occur.^{7, 86, 114, 118, 156, 157} Factors which interfere with and disrupt the normal intestinal flora, such as antimicrobial therapy and food and water deprivation, may enhance colonization and temporary overgrowth by salmonellas, especially in the small intestine.^{21, 50, 132} Colonization tends to occur more readily in stressed animals.^{7, 132}

The ability of the bacteria to attach to and invade enterocytes is essential for the development of enteric salmonellosis.⁷ Following oral infection of calves, Salmonella are recovered in high numbers from the distal ileal mucosa within the first 72 hours of infection, suggesting that this is the main site of invasion.¹⁴⁰ The possession of pili enables the bacteria to become attached to the surface of enterocytes, which facilitates their entrance into the cells through the brush border. The bacteria may also invade the mucosa through intercellular junctional complexes.⁷ Most salmonellas remain intact within membrane-bound vacuoles in the cytoplasm of enterocytes, where they multiply and produce enterotoxin.⁷ Although many bacteria may be present in a single enterocyte during the early stages of infection, cellular damage is mild.^{7, 156} After 24 hours of infection most of the bacteria are located in membrane-bound vacuoles within macrophages and neutrophils in the lamina propria^{7, 21} from whence they may spread to the regional lymph nodes, in which further multiplication takes place.

Stimulation of secretion of increased amounts of fluids and electrolytes

Enterotoxin and the inflammatory response that follows invasion of the intestinal mucosa by salmonellas^{87, 124, 132} causes the release of prostaglandins that activate mucosal adenyl-cyclase, resulting in a net secretion of water, Na⁺ , HCO₃ ^-; , and Cl^-; into the lumen of the intestine.^{87, 109, 133} Malabsorption and maldigestion develop as a result of cellular infiltration in the affected intestine and damage to the villi, which restricts lymph and blood flow and diminishes the absorptive surface.¹⁰⁹

The role of virulence factors that are associated with septicaemic salmonellosis, including the lipid A portion (endotoxin) of the cell wall lipopolysaccharide, is discussed in the introduction to Salmonella spp. infections. ^{7, 87} For more information on the composition and pathophysiological effects of endotoxin, consult the section on pathogenesis in Escherichia coli infections.

The relative roles of cell-mediated and humoral immunity in protection against, and recovery from, salmonellosis are not well understood,¹⁹ but both are probably involved.^{14, 24, 64, 65}

Clinical signs

In cattle, the enteric and septicaemic syndromes of salmonellosis aremore common^{2, 105, 145} than the abortion syndrome.⁵² One ormore of the syndromes may occur simultaneously in an outbreak of salmonellosis in a herd, or even in a single affected animal.¹⁵⁶ Salmonella Dublin is more often the cause of septicaemia than S. Typhimurium,^{2, 93} and adult animals are less likely to suffer from septicaemia.⁷

Calves

Calves may develop peracute, acute or chronic salmonellosis.¹⁰⁹

The peracute disease is usually a septicaemic condition. It is often fatal, and calves may die suddenly without being seen to be ill.¹⁰⁹ Some, however, develop enteritis and diarrhoea in addition to septicaemia.^{2, 145} When the course of the septicaemia is protracted, signs of hepatitis, pneumonia, meningoencephalitis, polyarthritis and osteomyelitis may develop.^{2, 13, 93, 99.105}

Acute enteric salmonellosis is the most common syndrome of salmonellosis encountered in calves.^{2, 5, 109, 156} Following an incubation period whichmay vary from one to five days, calves develop a high fever,¹⁵⁸ inappetence, lethargy and depression, diarrhoea, polypnoea and frequently a serous nasal discharge followed by a slight cough.^{93, 112, 114, 118} Scouring may only occur terminally.¹⁰⁷ The faeces of affected calves are foulsmelling, have a putty-like consistency and contain large amounts of mucus, sloughed mucosa and flecks of blood.^{2, 114, 118} These animals show signs of colic, become gradually weaker, are unthrifty and dehydrated and may collapse into sternal recumbency. At this time the body temperature may be normal or subnormal.¹⁵⁷ Calves that die probably develop a terminal septicaemia.¹¹⁸ The morbidity rate is generally much higher among purchased than home-bred calves; it may reach 75 per cent, but mortality rates are generally between 5 and 10 per cent.

Chronic salmonellosis in calves is characterized by unthriftiness, long and scruffy hair coats and stunting.^{109, 156} Diarrhoea is not always present and signs of chronic pneumonia with persistent coughing may occur.^{61, 109}

Calves that survive either peracute, acute or chronic disease may develop pneumonia, meningoencephalitis, purulentpolyarthritis (particularly of the carpal and tarsal joints), and osteomyelitis of the vertebrae and bones of the distal parts of the limbs, resulting in lameness, paresis or even almost complete paraplegia.^{40, 70, 99, 109, 135}Dry gangrene of the skin of the lower limbs (often between the carpus/tarsus and the coronary band) and the tips of the ears and tail, resembling ergotism, is rarely seen with S. Dublin infection.^{40, 88, 105} The affected parts are cold and sharply demarcated from the normal tissues.

Adult cattle

Adult cattle generally contract either acute or subacute enteric salmonellosis, and pregnant animals may abort.^{66, 145, 151, 156}

During the early stages of the acute enteric disease, severely affected animals show fever, depression, inappetence, and a drop in milk yield. These signs are followed by diarrhoea which is foul-smelling, the faeces being mucoid and usually containing clots of blood and shreds of necrotic intestinal mucosa.^{17, 105, 122} Signs of colic, congested mucous membranes and dehydration may be evident.¹⁰² The acute disease lasts for about a week. The case fatality rate in adult animals with dysentery is usually about 50 per cent, but may be higher.^{104, 108} Complete recovery may take up to two months.^{60, 145}

Similar but less severe signs are present in animals suffering from subacute enteric salmonellosis,^{122, 145} and most affected animals recover without treatment.¹⁴⁵

Salmonella Dublin in particular, but also S. Typhimurium and other serovars, may cause abortion in cows at any stage of pregnancy.^{44, 52, 54, 66} Abortions may either precede the onset of dysentery or follow it within two to four weeks. Alternatively, abortion may follow a period of pyrexia or it may be the only sign of ill health.^{42, 54, 60, 108} Aborted foetuses generally show evidence of decomposition.⁴³ Retention of the placenta occurs in approximately 70 per cent of cows that abort but subsequent fertility is not usually affected.^{42, 44} Salmonella Brandenburg abortions are being recognized with increasing frequency in New Zealand.²⁰

Humans

In humans, a number of disease syndromes are caused by infection with salmonellas. These include food poisoning characterized by diarrhoea and vomition, septicaemia, arthritis, meningitis, and pustular dermatitis on the arms and hands of animal handlers and veterinarians who perform obstetrical manipulations on infected cows.^{4, 13, 32, 52, 77, 137}

Pathology

Calves suffering from peracute septicaemic salmonellosis show a marked leukopenia with a left shift. Metabolic acidosis may be present, even in the absence of diarrhoea or dehydration.¹⁰⁹

In calves with enteritis, leukopenia is present during the early stage, but those that survive for three to four days develop a leukocytosis and elevated plasma fibrinogen levels. During the initial stage of enteric disease, dehydration results in elevated packed cell volume and plasma protein levels, but plasma protein levels drop after some time due to loss into the gastrointestinal tract.^{109, 118, 142} Diarrhoeic calves have decreased serum sodium and chloride levels, and serum potassium values may be either elevated or depressed, despite the tendency towards a metabolic acidosis.^{109, 149} Blood urea levels can increase markedly and may be of value in prognostication.¹⁴⁹ Plasma bilirubin levels are raised in calves with cholestasis possibly because of an interference in bilirubin excretion by bacterial metabolites.¹⁴²

Calves that have died from peracute septicaemic salmonellosis usually have widespread subcutaneous, mucosal and serosal petechial haemorrhages, generalized congestion, oedema and congestion of the lungs, splenomegaly and hepatomegaly.^{7, 109, 142}

The carcasses of calves that have died from the acute enteric disease reveal varying degrees of dehydration and in some cases mild icterus.^{142, 145, 157} There is moderate hepatomegaly, and the liver is bronze or orange-brown and often has a few to numerous greyish-white foci of necrosis, 0,5 to 1,0 mm in diameter, as well as a few petechiae disseminated throughout the parenchyma.^{49, 142} In order to see the necrotic foci with the naked eye, it is often necessary to examine several cut surfaces of the liver very carefully in good light, sunlight being preferable. The gall bladder is distended, the wall is oedematous and there may be focal necrosis of its mucosa or haemorrhages in the wall.¹⁴² The spleen is moderately enlarged and on cut section may reveal inconspicuous necrotic foci in the red pulp, similar to those in the liver.⁷ Small areas of acute bronchopneumonia (sometimes accompanied by haemorrhages in the lung parenchyma and a fibrinous pleural exudate) and swelling of the kidneys with whitish-grey foci of necrosis (0,5 to 1,0 mm in diameter) in the renal cortex may be evident in some animals.^{7, 142, 145} The lesions in the gastrointestinal tract vary in severity and location. In S. Dublin infections the abomasal musosa may have multiple erosions and petechiae.¹⁰⁹ In most calves with salmonellosis the jejunum and ileum are affected. Depending on the severity of the disease, catarrhal, necrotizing or diphtheritic jejunitis and ileitis may be present.^{7, 110, 114, 156} In some animals the caecum and colon show similar lesions to those in the small intestine. The contents of the intestine, particularly the affected parts, are watery, foul-smelling and usually contain copious amounts of an admixture of fibrin, mucus, desquamated mucosa and digested blood.¹⁵⁶ The mesenteric lymph nodes are invariably enlarged and oedematous, and may reveal petechiae on cut surface.

The carcasses of calves that have died from the chronic disease manifest many of the lesions present in the acute disease although the large intestinal lesions are often more discrete and necrotic.¹⁰² In addition, there are frequently signs of localization of the infection in a variety of organs and tissues.¹⁰⁹ These include fibrinopurulent synovitis of the larger joints (particularly of the limbs), fibrinopurulent bronchopneumonia and abscessation in the lungs, and occasionally meningoencephalitis, osteomyelitis of one or more of the vertebrae and bones of the limbs, and ischaemic necrosis of the skin of the tips of the ears and the distal parts of the tail and limbs.^{70, 88, 99, 109, 145}

The histopathological lesions in the liver comprise small foci of coagulative necrosis which are infiltrated by a few macrophages and mononuclear cells.⁷ These foci are present in most livers and are referred to as ‘typhoid nodules’.They are randomly scattered in lobules throughout the liver, some of which are associated with thrombosis of central veins or blood vessels in portal triads.¹⁴²

Other lesions include mild to moderate infiltration of mononuclear cells into most portal triads, vasculitis sometimes accompanied by thrombosis of some of the larger blood vessels in the triads, moderate Kupffer cell proliferation, clumps of Gram-negative bacteria in sinusoids and bile stasis.¹⁴² Vascular lesions and necrotic foci similar to those in the liver are usually present in the spleen and sometimes also in the lungs, lymph nodes (particularly the mesenteric lymph nodes), kidneys and bone marrow.⁷ The lesions in the affected parts of the intestines are characterized by necrosis and ulceration of the mucosa, presence of moderate numbers of mononuclear cells and neutrophils in the lamina propria and submucosa, and vasculitis and thrombosis of some of the blood vessels in the submucosa. Copious amounts of cellular debris, mucus and fibrin adhere to the necrotic mucosa or are present in the lumen of the affected parts of the intestines. Salmonellas may be observed microscopically as individual bacteria or colonies of organisms, associated with the areas of inflammation and necrosis.¹⁴²

The macro- and microscopic lesions of salmonellosis in adult cattle are similar to those in calves except that the enteritis is generally more haemorrhagic and fibrinous or necrotic.^{7, 66, 122} Cows with mammary infections may have a chronic-activemastitis and supramammary lymphadenitis.¹²⁰ A purulent endometritis and necrotic hepatic foci may be seen in cows that abort.⁴⁴ The chorioallantois is thickened, the chorionic surface is mottled red and grey and cotyledons, which are tan or red, may be covered with a yellow exudate. The latter may contain remnants of maternal caruncle.⁶⁹ Histologically, mineralization of areas of the placenta may be extensive, and some villimay contain large numbers of neutrophils.⁶⁹ Many cotyledonary villi are necrotic and capillaries in the chorionic arcade contain prominent bacterial colonies; the cotyledons contain more bacteria than do caruncles.⁴⁴ The foetal liver can have multiple foci of suppuration while the lungs are generally normal. Occasionally, however, neutrophilsmay be seen in the bronchi and bacteriamay colonize the bronchial epithelium.⁶⁹

Diagnosis

The diagnosis of salmonellosis is based on the isolation of the causative organism, supported by the history, clinical signs and lesions at necropsy.^{2, 122} Specimens submitted to the laboratory for Salmonella isolation should be incubated in selective enrichment media to enhance the chances of isolating the organisms (see the introduction to Salmonella spp. infections).

In live animals with diarrhoea, faecal specimens (2 to 20 g) or rectal swabs should be submitted for bacterial isolation.^{40, 95, 145, 156} In animals suffering from severe diarrhoea, the large volume of faeces may dilute the number of organisms in the faeces to such an extent that rectal swabs contain insufficient organisms to enable successful isolation.^{109, 119}

Salmonellas may be isolated from the blood of septicaemic animals.^{114, 122, 142, 145, 156}

Apart from the examination of faecal specimens and rectal swabs, rectal mucosal biopsy provides an easy and safe method that increases the chance of isolating Salmonella organisms,⁹⁵ the reason being the adherent and invasive nature of salmonellas that results in their concentration on the mucosa.⁹⁵

From dead animals, specimens of liver and spleen, one or more mesenteric lymph node (particularly the ileal and/or colonic), and a section of the affected part of the intestine (e.g. ileum and/or colon) should be submitted at 4 °C for bacterial isolation.¹¹⁸ In addition, specimens from the liver, spleen, kidneys, brain, lungs and intestine should be collected and placed in a 10 per cent buffered formalin solution for histopathological examination. The presence of the typical necrotic foci and thrombosis, particularly in the liver and spleen, are highly suggestive of salmonellosis.

The identification of carrier animals is not always easy, as such animals may shed bacteria intermittently and it may be necessary to examine specimens taken from them on a number of occasions before a positive culture is obtained.¹⁵⁶ The identification of latent S. Dublin carriers is a major problem, as faecal culture and serology are usually negative.¹⁶¹ Since parturition may activate a latent infection, swabs of faeces and vaginal discharges should be cultured.^{23, 103} Where a latent infection is suspected in a dead animal, special attention should be paid to attempting to isolate salmonellas from the gall bladder, ileocaecal lymph nodes, tonsils, female genital tract, supramammary lymph nodes and udder.^{73, 103, 119, 120, 148}

Salmonellas can be isolated from the organs (liver, spleen, lungs) and abomasal contents of aborted foetuses.⁵² The placenta and vaginal mucus of cows that abort should also be submitted for bacterial isolation.^{104, 145}

Serological tests, such as ELISA, serum agglutination and complement fixation,^{15, 74, 120, 156} can be used for the retrospective diagnosis of salmonellosis or the detection of carriers. These tests are, however, rarely used for diagnostic purposes and are only reliable when applied on a herd or flock basis, or when both acute and convalescent phase sera are tested.^{102, 132} Antibody responses are much more consistent in animals that have suffered systemic infections, i.e. bacteraemia or septicaemia.^{54, 132} Many infected animals may not have positive titres, either because the serum was collected too early during the course of infection (less than 14 days) or because the infection was not severe enough to stimulate a detectable humoral immune response.^{40, 102, 132} Latently infected cattle remain serologically negative.⁷⁴

ELISAs have been developed primarily for the detection of S. Dublin or S. Typhimurium carriers;^{58, 59} but, due to cross-reacting O antigens, the specificity has been poor.^{57, 71} More specific assays have been developed to identify S. Dublin carriers using fimbrial antigens⁵⁷ or serogroupspecific lipopolysaccharide.⁷¹

ELISAs have been used to detect antibodies in both blood and milk.^{58, 59, 71}

Differential diagnosis

The clinical signs of enteric salmonellosis in calves are nonspecific and are very similar to those caused by many other infectious and non-infectious agents that affect the gastrointestinal tract. The most important of these include viruses (e.g. rota-, corona-, Breda- and BVD viruses), bacteria (e.g. Escherichia coli, Clostridium perfringens types A, B or C, Yersinia spp., Chlamydophila (Chlamydia) spp.), protozoa (e.g. Eimeria spp., Cryptosporidium sp.) and nutritional causes (over-feeding, incorrect feeding and the feeding of milk-replacers containing heat-denatured whey proteins).^{49, 102, 109} The clinical signs and lesions of salmonellosis in calves may be very similar to those of Rift Valley fever.

The diarrhoea associated with enteric salmonellosis in adult cattle may be bloody or dysenteric and should be differentiated from that caused by BVD virus, arsenic poisoning,¹⁰² helminths (e.g. Geigeria pachyscelis, Bunostomum phlebotomum, and Paramphistomum microbothrium), toxic plants (e.g. Ornithogalum spp., Ornithoglossum spp., Homeria and Moraea spp., Quercus spp. and Pteridium spp.) and ingestion of the pollen beetle (Astylus atromaculatus).⁶⁷

Abortion caused by Salmonella serovars should be differentiated from that induced by other agents, the most important of these in southern Africa being Brucella abortus, Leptospira serovars, Rift Valley fever virus, BVD virus and Palyam serogroup viruses.

Control

Different approaches to the therapy of salmonellosis, particularly the enteric disease, have been reported.^{68, 109} The use of antimicrobial drugs in the treatment of enteric salmonellosis, although controversial, may have beneficial effects, especially if applied during the early stages of the disease.^{3, 60, 68, 109} Parenteral antimicrobial therapy has been shown to be more beneficial than oral treatment.¹⁰⁹ Antimicrobial drugs have been shown to be effective in preventing the development of bacteraemia or septicaemia in animals suffering from enteric disease.⁹¹ They also prevent localization of Salmonella in extra-intestinal organs and the subsequent development of lesions.^{7, 109}

Antimicrobial drugs generally recommended for parenteral use are ampicillin, amoxycillin, gentamicin, trimethoprim-sulfonamide combinations and fluoroquinolones.^{30, 91, 102, 109, 143} Salmonella Dublin is sensitive to most antimicrobials¹⁵² although increasing antibiotic resistance in this serovar is being recognized in the USA;³³ strains of S. Typhimurium, particularly phage types DT104, DT193 and DT204C in the UK, however, have shown increasing resistance to a range of antimicrobials (see Aetiology, above).

An antibiogram will be of help to the practitioner, because antimicrobial sensitivity may vary geographically.⁶⁸ Resistance is higher in bacteria isolated from calves than in those isolated from adult cattle, which may be related to the increased use of antimicrobials in calves.⁷⁸

The oral administration of antimicrobial drugs in cattle is a satisfactory method of treatment,¹⁰² but it must be used with caution.⁸⁴ Some antimicrobial drugs, e.g. neomycin, chloramphenicol, tetracycline and ampicillin, may cause signs of diarrhoea due to malabsorption after three days of treatment.⁸⁴ Disturbance of the gastrointestinal flora by the use of antimicrobial drugs in the presence of resistant Salmonella may result in overgrowth of these organisms and the conversion of an enteric infection into a septicaemic form. Antimicrobial drugs administered orally may also increase colonization of the gut by other Gram-negative bacteria, induce the development of multiple drug resistance, and prolong the carrier state.^{34, 35, 111, 121, 129}

Antimicrobial therapy does not usually eliminate the carrier state in cattle.^{68, 102} The number of animals that shed the organism and the duration and amount of shedding may be increased if the Salmonella strain involved is resistant to the drug used.¹⁰² Chloramphenicol facilitates the persistence of salmonellas, particularly the antimicrobialresistant serovars.^{79, 94, 131}

It is generally agreed that supportive therapy and good nursing are important. These include oral or parenteral rehydration, correction of electrolyte imbalance and stabilization of the acid-base equilibrium. Symptomatic treatment with opioids, alpha-2-agonists, parasympatholytics and anti-inflammatory drugs may have a beneficial effect.¹³⁶ Non-steroidal anti-inflammatory drugs, such as flunixinmeglumine,may be of benefit in cases with endotoxic shock and to block intestinal prostaglandin production.⁶⁸ Most anti-inflammatory drugs are, however, potentially dangerous especially in dehydrated animals.¹³⁶ There is no consensus on the value of intestinal adsorbents and protectants, such as activated charcoal and kaolin, in animals affected by enteric disease.⁶⁸

In programmes designed to control salmonellosis, the measures described below should be applied.

Measures aimed at protecting cattle

Risk factors over which the farmer can exert a level of control include purchasing replacement stock from direct sources rather than dealers, quarantine of purchased animals for a four-week period, housing sick animals in dedicated isolation areas, preventing wild bird access to cattle feed stores, and vaccination. These measures are likely to have the greatest impact on the reduction of salmonellosis, including disease due to multiple-resistant S. Typhimurium DT104 in the cattle population.^{1, 31} Improving the resistance of animals in high-risk groups by immunization is important, as is correct feeding to maintain the intestinal flora in a balanced state. Separation of age groups and the prevention of contact with other infected carrier animals lessen the risk of exposure; while the isolation of diseased animals and the elimination of potential sources of infection prevent the spread of the infection and the contamination of the environment.

Measures aimed at the agent

Treatment and isolation or elimination of animals suffering from salmonellosis, as well as disinfection of sheds and stables, should be implemented to prevent the build-up of environmental contamination. To eradicate S. Dublin from dairy herds, every effort needs to be made to detect carrier animals so that they can be culled.¹²⁰ Salmonella bacteria are destroyed by most disinfectants that are effective against vegetative bacteria. Some specific disinfectants, e.g. diethylpyrocarbonate + hydrogen peroxide, are recommended for use in feedstuffs¹⁰¹ but are generally too expensive to use as disinfectants for the external environment or fomites. Salmonella-contaminated areas, such as stables, concrete areas, equipment and vehicles should be steam-cleaned and then disinfected with phenolic-, chlorine- or iodine-based disinfectants.^{51, 68, 119} Yards with earthen flooring can be decontaminated with several successive sprayings of 5 per cent formalin.⁸³ Carcasses of infected animals should be burnt and should definitely not be rendered for animal feed. Slurry should preferably be used on crops (other than root crops) and not pastures intended for grazing. Silage making destroys salmonellas.¹⁰²

Measures aimed at the environment

These include the institution and maintenance of hygiene and good animal husbandry practices, such as the regular removal of faeces;⁴⁰ keeping food stores rodent-free; the use of separate milk pails, which are thoroughly washed and disinfected after use, for each calf; provision of suitable housing; and the prevention of overcrowding. In order to break the cycle of infection, consideration should be given to an all-in all-out policy with thorough cleaning and disinfection between batches of calves.⁵⁵ Any procedure likely to enhance aerosol transmission should be avoided.⁵⁵

Vaccination

The use of vaccines is important in the control of salmonellosis in cattle, but immunization on its own is often insufficiently effective²³ to be relied upon entirely, and other means of limiting the spread of infection (such as those described above) also need to be implemented.¹⁶¹

Generally, both live attenuated vaccines produced from rough strains and bacterins precipitated on aluminium hydroxide are available commercially. The Onderstepoort Biological Products produces two vaccines against bovine salmonellosis:

• a trivalent, formalin-inactivated bacterin prepared from isolates of S. Dublin, S. Typhimurium and S. Bovismorbificans, and
• a live, attenuated vaccine containing an avirulent rough mutant of S. Dublin.

Live attenuated vaccines should be administered as a single inoculation to calves at two to four weeks of age.¹⁰² Antimicrobial drugs should not be administered to calves during the week prior to and for two weeks after immunization with live attenuated Salmonella vaccines, as immunity is dependent upon the multiplication of the bacteria contained in the vaccine.

Bacterins, to be effective, need to be administered twice at an interval of two to four weeks but are usually ineffective in calves under six weeks of age. For this reason, the administration of bacterins to pregnant cows is sometimes recommended in order to provide their calves with colostral immunity, which persists at protective levels for approximately six weeks.¹⁰² On farms on which calf salmonellosis is a particular problem, calves whose dams were immunized with a bacterin during pregnancy should be immunized at six weeks of age with a live attenuated vaccine against S. Dublin. In this way it is usually possible to ensure that these calves have an adequate level of immunity during the danger period, viz. 3 to 12 weeks of age.

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