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Letter to Editor

A nosocomial, foodborne outbreak of Salmonella Enterica serovar

Enteritidis in a University hospital in Greece: the importance of

establishing HACCP systems in hospital catering.

A. Gikasa*, E.I. Kritsotakisa, S. Marakia, M. Roumbelakia, D. Babalisb, E. Scoulicaa, C.

Panoulisa, E. Saloustrosb, E. Kontopodisb, G. Samonisb and Y. Tselentisa

a
Department of Clinical Bacteriology, Parasitology, Zoonoses and Geographical Medicine,

University Hospital of Heraklion, Greece

b
Department of Internal Medicine, University Hospital of Heraklion, Greece

*Correspondence to:

Achilleas Gikas,

University Hospital of Heraklion-1352,

GR71110, Crete, Greece.

E-mail: gikas@med.uoc.gr; gikasa@infection.gr

Tel.: +30-2810-375050,

Fax: +30-2810-392847
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Madam,

Nosocomial outbreaks of salmonellosis frequently result from breakdowns in food safety

control measures in hospital catering.1,2 We report briefly the first nosocomial, foodborne,

outbreak of salmonellosis in a 750-beds University hospital in Greece.

On 20 July 2005, 12 febrile gastroenteritis cases among inpatients and employees

were reported to the infection control team. Prompted control measures included patient

isolation, exclusion from work of symptomatic staff and enhanced surveillance to detect new

cases. A case was defined as any person staying or working at the hospital who presented

diarrhoea and/or fever, plus one other gastrointestinal symptom, with onset after 16 July.

A total of 133 cases were identified, including 86 (65%) inpatients, 31 (23%) visitors,

and 16 (12%) employees. Their median age was 60 years and 67% were female. Main

symptoms included diarrhoea (94%), abdominal pain (75%), fever (77%), chills (56%),

vomiting (35%), nausea (14%), and myalgia (13%). Cases presented a wide spatial

distribution, and their temporal clustering (19-22, July) suggested a point-source outbreak. A

case-control study, comparing food exposures between 110 cases and 97 randomly selected

controls, subsequently showed that illness was associated with consumption of roast chicken

(OR = 23.9, P<.001), spaghetti (OR = 13.4; P<.001) and cheese (OR = 4.5; P<.001). All

items had been served as dinner on 19 July.

Salmonella Enterica serovar Enteritidis (S. Enteritidis) was isolated in 64 faecal and 6

blood specimens from case-patients. Additionally, 3/47 stool samples from catering staff

were positive, including two asymptomatic food-handlers. S. Enteritidis was also isolated

from processed cheese that was stored in refrigerators and was used to prepare the implicated

dinner. However, it was not cultured from intact cheese, indicating contamination during
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processing. All other samples (including raw foods stored in refrigerators, foods prepared on

21 July, inert surfaces, utensils, and tap water) were negative for enteric pathogens. However,

Staphylococcus warnerii and Staphylococcus haemolyticus (>25 cfu/g) were detected in

cooked foods and unacceptable levels of coliforms (>180cfu/20cm2) were detected on

surfaces and utensils. All S. Enteritidis isolates were sensitive to all antibiotics tested, had the

same antibiogram pattern and were identical at pulsed-field gel electrophoresis and

ribotyping, confirming a clonal outbreak.

An inspection of kitchen facilities and hygiene practices on 21 July revealed key

faults, mainly including non-systematic use of gloves and gowns, processing of raw foodstuff

on common surfaces using the same equipment, and absence of written guidelines for

cleaning and disinfection of kitchen equipment.

Of the 120 case-patients (90%) who were evaluated until discharge, 15 (12.5%)

presented complications: 6 (5%) septicaemia; 8 (6.7%) renal function impairment; and 1

patient (0.8%) developed a mild pancreatic reaction. Two of the patients with septicaemia

presented decompensation of serious underlying diseases and subsequently died. However,

other complications, such as metastatic infections and abscesses, were not observed.3 We

assume this is due to the early and extended use of quinolones, which may also have

contributed to the control of the outbreak and the prevention of secondary cases, through the

rapid interruption of faecal shedding.3

Cross-contamination between the implicated foods, via kitchen equipment, was an

underlying factor in this outbreak, but the ultimate cause, or how kitchen equipment became

contaminated, can only be speculated. This may have occurred due to a small supply of

contaminated poultry that escaped routine bacteriological sampling, but the possibility that

infected food-handlers were the source of contamination cannot be excluded.4 In either case,
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S. Enteritidis would have readily been transferred to hands and utensils, given the key faults

that were noted in food-handling practices. In association with inadequate temperature

control and/or inadequate cooking, this may have led to a substantial increase of the S.

Enteritidis load in foods (Figure 1).

In our hospital, as in most hospitals, food hygiene and safety efforts are directed

towards the conventional approach of inspection of food-handling practices, end-product

bacteriological sampling and routine faecal screening of food-handlers.5 However, it has been

emphasized that this approach is not cost-effective and may not reduce the risk of foodborne

outbreaks.6

In contrast, the value of introducing the Hazard Analysis Critical Control Point

(HACCP) system in hospitals has been noted.5,7 HACCP offers advantages over conventional

end-point testing, which include the identification of potential hazards before they occur, its

application to the whole process rather than just the areas sampled, and the high degree of

involvement of all catering staff that reinforces their knowledge and interest in improving

practices.5,8 However, few studies have looked at the extent of implementation of, and

adherence to, the HACCP approach in hospitals.8 An audit of 99 hospitals in Greece,

performed in 2003 by the Hellenic Food Authority, revealed that only 4 hospitals had

established a HACCP system (personal communication). In our hospital, the outbreak

accelerated administrative decisions to implement HACCP, which is now fully operational.

This outbreak is a reminder of the impact of nosocomial salmonellosis and the

importance of ensuring that high quality standards of food processes are applied to food

destined for hospital populations. The significance of HACCP implementation needs to be

clarified and emphasized in hospital catering.

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References

1. McCall B, McCormack JG, Stafford R, Towner C. An outbreak of Salmonella

typhimurium at a teaching hospital. Infect Control Hosp Epidemiol 1999;20:55-56.

2. Sion C, Garrino MG, Glupczynski Y, Avesani V, Delmee M. Nosocomial outbreak of

Salmonella enteritidis in a university hospital. Infect Control Hosp Epidemiol

2000;21:182-183.

3. Hohmann EL. Nontyphoidal salmonellosis. Clin Infect Dis 2001;32:263-269.

4. Meakins SM, Adak GK, Lopman BA, O'Brien SJ. General outbreaks of infectious

intestinal disease (IID) in hospitals, England and Wales, 1992-2000. J Hosp Infect

2003;53:1-5.

5. Richards J, Parr E, Riseborough P. Hospital food hygiene: the application of Hazard

Analysis Critical Control Points to conventional hospital catering. J Hosp Infect

1993;24:273-282.

6. Khuri-Bulos NA, Abu Khalaf M, Shehabi A, Shami K. Foodhandler-associated

Salmonella outbreak in a university hospital despite routine surveillance cultures of

kitchen employees. Infect Control Hosp Epidemiol 1994;15:311-314.

7. Shanaghy N, Murphy F, Kennedy K. Improvements in the microbiological quality of

food samples from a hospital cook-chill system since the introduction of HACCP. J

Hosp Infect 1993;23:305-314.

8. Angelillo IF, Viggiani NM, Greco RM, Rito D. HACCP and food hygiene in

hospitals: knowledge, attitudes, and practices of food-services staff in Calabria, Italy.

Collaborative Group. Infect Control Hosp Epidemiol 2001;22:363-369.

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Figure 1
Hypotheses on the source of infection and chain of transmission in the outbreak of S. Enteritidis at the University Hospital of Heraklion,
Greece, 2005

Hypothesis 1:
S. Enteritidis entered
the kitchen from
outside the hospital,
via contaminated raw
food material (e.g.
poultry)
Inappropriate Dissemination Food cross-
food handling of S. Enteritidis contamination
AND/OR PLUS procedures in kitchen via kitchen
and/or equipment equipment
poor hygiene and/or and/or
Hypothesis 2: practices worker’s hands worker’s hands
S. Enteritidis entered
the kitchen from inside OUTBREAK
the hospital, via PLUS
infected personnel
(asymptomatic food
handlers not excluded
Increase of S.
from work)
Enteritidis load in
foods due to
inadequate
temperature
control and/or
cooking