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Two human cases of Salmonella typhimurium DT104 linked with raw milk consumption
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Prof C Bradley, ICGP
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Dr P McKeown, HPSC
Dr L Thornton, FPHMI
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M Kelly, HPSC
(Editor)

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Two human cases of Salmonella typhimurium DT104 linked with raw milk consumption

Summary

An outbreak of Salmonella Typhimurium definitive type (DT) 104 occurred in a dairy farming family in Leinster during the Autumn of 2010. Following a detailed public health investigation, the outbreak was attributed to the consumption of raw milk on the family farm. A number of days prior to the family outbreak, several milking cows had clinical signs of enteric disease. A tentative diagnosis of salmonellosis was made by the farm’s private veterinary practitioner (PVP) and subsequently this diagnosis was confirmed on faecal culture at a Department of Agriculture, Fisheries and Food (DAFF) Regional Veterinary Laboratory. The isolates were sent to the National Salmonella Reference Laboratory (NSRL) for subtyping. Multi-locus variable number of tandem repeat analysis (MLVA) patterns and antimicrobial resistance (AMR) profiles of both human and bovine isolates were indistinguishable.

This outbreak highlights the health risks associated with the consumption of raw milk.

Public Health Investigation

The Department of Public Health (HSE-East) was notified by a laboratory of a confirmed case of Salmonella group B on 22/10/2010. The case was a farmer in his 30s with a history of diarrhoea, fever and abdominal pain. He reported that three other household family members had similar symptoms and were advised to seek further medical attention. He informed his doctor that a number of milking cows in his dairy herd had been diagnosed with salmonellosis. The family were advised to take precautionary measures to avoid infection, including discontinuing the practice of drinking raw milk.

A second case of Salmonella Group B in the extended family was notified to the department on the 11/11/2010. The case was a young female relative of the index case.  She was not a farm resident, nor did she have any contact with animals or the general farmyard environment, but she had consumed raw milk on a visit to the farmhouse. Her symptoms occurred at the same time as those of the index household. She was initially seen by her general practitioner and was investigated when her symptoms persisted.

Animal Health Investigation

A number of days prior to the family outbreak, several milking cows from the herd had clinical signs consistent with a diagnosis of salmonellosis. Faecal samples were sent by the farms PVP to the regional veterinary laboratory and were received on 18/10/2010.  Salmonella Typhimurium DT 104 was isolated. The PVP and consequently the farmer involved were informed. The local District Veterinary Office was notified. Appropriate control measures were put in place on the farm. The family were advised to take a number of hygienic precautions to avoid infection and to stop drinking raw milk.  

The NSRL in University College Galway typed isolates from both bovine and human cases. The MLVA patterns and AMR profiles were indistinguishable.

Bovine Salmonellosis

The two most common serotypes causing bovine salmonellosis are Salmonella Dublin and S. Typhimurium. S. dublin is highly adapted to cattle but may cause disease in humans.   S. Typhimurium lacks host specificity and can infect and cause disease in a variety of animals and humans1. In 2009 S. dublin accounted for 93% of the bovine diagnostic samples that tested positive for salmonella in Ireland's regional veterinary laboratories. S. Typhimurium was a sporadic finding accounting for less than 1% of this particular group of salmonella isolates2. Although salmonellosis affects cattle of all ages, the disease is most severe in calves and stressed adults in herds with chronic infections (endemic herds), and at all ages in naïve herds with no previous exposure. A cow or calf undergoing an active infection sheds large numbers of salmonella from body secretions and excretions (faeces, urine, saliva and milk) contaminating the environment directly, including feed and water supplies, streams, rivers and pastures. Salmonella infections may manifest as enteritis, systemic disease or abortion. Milk is most likely to become contaminated by faeces from either an animal with clinical salmonellosis or a healthy carrier animal during the milking process. Mammary excretion of salmonella is more likely during the febrile stage of disease.

One of the differences between the diseases caused by S. Dublin and S. Typhimurium is the marked tendency for S. Dublin to persist in adult cattle and create a significant reservoir of carrier animals. S. Typhimurium does not do so as much, so the disease is likely to subside after an initial exposure and to recur only when the source of infection, such as birds, rodents, feedstuff, sewage or slurry reappears. However, persistence at farm level for prolonged periods, including intermittant excretion in the milk of clinically normal cows has been documented3,4,5,6. Recognition of such an occurrence has important consequences for animal and human health6.    

Other examples of outbreaks associated with the consumption of unpasteurised milk

In the 10 year period between 1970 and 1979, there were 29 outbreaks of salmonella food-poisoning recorded in Scotland affecting 2428 persons who had consumed raw milk.  Eleven of the outbreaks were restricted to farm workers and their families resident on or near dairy farms. The other 18 episodes were more widespread in the general community and affected an estimated minimum of 2290 persons who had consumed “premium” or “standard” grade raw milk from producer-retailer dairy farms7. Subsequently in 1986, sales of unpasteurised milk bottled on farms direct from farms and local retailers were prohibited. In 2004 the existing ban on raw cow’s drinking milk and raw cream was extended to all species8.

From 1 January 1992 to 31 December 2000, 27 milkborne general outbreaks of infectious intestinal disease were reported to the public health laboratory service (PHLS) Communicable Disease Surveillance Centre(CDSC) in the United Kingdom. These outbreaks represent a fraction of all outbreaks of foodborne origin (N=1774) reported to the CDSC, but were characterised by significant morbidity. Unpasteurised milk was the most commonly reported vehicle of infection in milkborne outbreaks. Salmonella spp (37%), vero cytotoxin-producing Escherichia coli (VTEC) 0157 (33%) and Campylobacter spp. (26%) were the most commonly detected pathogens, and most outbreaks were linked to farms (67%)9.

In the largest outbreak of VTEC 0157 infection in England and Wales to date, 114 people were ill and 28 people were admitted to hospital in February 1999 following the consumption of improperly pasteurised milk from a local dairy in North Cumbria. A separate outbreak of VTEC lasted 13 days and was associated with the consumption of unpasteurised milk. Seven people were affected, four were admitted to hospital, and three developed haemolytic uraemic syndrome that required renal dialysis10.

In 2005, there was an outbreak of tuberculosis affecting cattle and people on a dairy farm in the southeast of Ireland, following consumption of milk from a seven year old cow with tuberculous mastitis. In this family, TB had a very significant impact on the health of two young children and five of six family members were positive on the Mantoux test. The family collected milk from the bulk tank and consumed it without pasteurisation. Bovine tuberculosis has been an ongoing problem in Ireland  for many years. A national eradication programme commenced in 1954, in part as a consequence of public health concerns, leading to a substantial reduction in disease prevalence by the mid 1960s11. Although subsequent progress has slowed, herd incidence has remained at approximately 5% for some years.  A wide range of measures are in place to minimise transmission between animals and people12 and infection is now very rare. However, these measures do not address practices such as on-farm consumption of raw milk. 

Conclusion

The key food safety issue regarding raw milk is that it may contain low numbers of pathogenic bacteria. Although most healthy people will recover from raw milk related illness within a short period, individuals with weakened immune systems such as children, pregnant women, the elderly and those suffering from chronic debilitating illnesses are particularly at risk, and are more susceptible to severe or life-threatening infections.  The outbreak of S. typhimurium DT 104 in this case once again highlights the health risk associated with the consumption of raw milk. The most effective way to protect public health is to ensure that raw milk intended for direct human consumption is pasteurised.

Carol Nolan, Donal O'Mahony FSAI; Mary Conlon, Mary Ward, HSE; William Byrne, Central Veterinary Research Laboratory

Acknowledgements:

The authors would like to thank the NSRL and Henrietta Cameron from the Central Veterinary Research Laboratory 

References

  1. Radostits O, Gay C, Blood D, Hinchcliff K. Veterinary Medicine: A Textbook of the diseases of cattle, sheep, pigs, goats and horses. 2000; 809-827.
  2. National Reference Laboratory Salmonella, (Food, Feed and Animal Health). Annual Report 2009. Backweston Laboratory Complex.
  3. Lanzas C et al.  Transmission Dynamics of a Multidrug- Resistant Salmonella Typhimurium Outbreak on a Dairy Farm.  Foodborne Pathogens and Disease 2010; 7, (4): 467-474.
  4. Fone DL, Barker RM. Associations between human and farm animal infections with Salmonella typhimurium DT104 in Herefordshire.  Communicable Disease Report 1994;  4 (11) 136-140.
  5. Sharpe W, Rawson B. Persistent Salmonella typhimurium PT 104 infection in a dairy herd. Veterinary record 1992; 131, 375-376.
  6. Giles J, Hopper S, Wray C. Persistence of Salmonella Typhimurium in a large dairy herd. Epidem. Inf. 1989; 103, 235-241.
  7. Sharpe J, Patterson G, Forbes G. Milkborne salmonellosis in Scotland. Journal of Infection, 1980; 2, 333-340.
  8. Advisory Committee on Microbiological Safety of Foods. Health risks to the consumer associated with unpasteurised milk and unpasteurised cream for direct human consumption. 2010; 1-21.
  9. Gillespie I, Adak G, O’ Brien S, BoltonF. MIlkborne general outbreaks of infectious intestinal disease, England and Wales, 1992-2000. Epidemiol. Infect. 2003; 130, 461-468.
  10. Djuretic T, Wall P, Nichols G. General outbreaks of infectious intestinal disease associated with milk and dairy products in England and Wales: 1992-1996. CDR 1997; 7, (3), 41-48.
  11. Doran P, Carson J, Costello E, More SJ.  An outbreak of tuberculosis affecting cattle and people on an Irish dairy farm, following consumption of raw milk.  Irish Veterinary Journal  2009; 62, (6) 390-397.
  12. More S, Good M. The tuberculosis eradication programme in Ireland: A review of scientific policy and advances since 1988. Vet.Mic. 2006; 112, 239-251 
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