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The New Zealand Medical Journal

 Journal of the New Zealand Medical Association, 21-June-2002, Vol 115 No 1156

Geographically separate outbreaks of shigellosis in Auckland, New Zealand, linked by molecular subtyping to cases returning from Samoa
Philip C Hill, John Hicking, Jennifer M Bennett, Azeem Mohammed, Joanna M Stewart, Greg Simmons,
Abstract
Aims To investigate simultaneous outbreaks of Shigella sonnei gastroenteritis occurring in February 2001 at a health camp for socially deprived children and an elderly care facility.
Methods Those with symptoms were interviewed using standardised questionnaire. Cases were defined as having least three loose stools over a 24 hour period and stool samples requested. A case-control study investigating routes of transmission was performed at the health camp. Environmental investigations of food safety and hygiene were conducted at each facility.
Results At the camp, 15 (37%) students and 15 (28%) staff met confidence interval 1.0-16.3; p=0.05) and, for staff, eating case criteria. Contact with human faeces (OR 4.0; 95% camp food (OR 6.9; 1.0-5.0; p=0.06) were shown to be independent risk factors for illness. At the elderly care facility, four (19%) residents and four (25%) staff met case criteria. Molecular subtyping confirmed that the outbreaks were related to each other and to other cases in travellers returning from Samoa to Auckland and other New Zealand cities over a four month period.
Conclusions Molecular subtyping is of considerable use in communicable disease investigation, providing strong evidence for links between outbreaks. With expanded technological capability, New Zealand could perform routine molecular subtyping of selected organisms to improve the detection and the investigation of regional and inter-regional outbreaks of infection.

Shigella spp. are responsible for less than 5% of bacterial food borne notifications in New Zealand. However, outbreaks of shigellosis are difficult to control because of the low infectious dose of the inoculum.1 Usually due to S. sonnei in developed countries,2 they have been reported most commonly among children at summer camps for the developmentally disabled3 and at daycare facilities.4
In February 2001, Auckland District Public Health Unit (PHU) was notified of two outbreaks of Shigella sonnei Biotype a gastroenteritis. One was at a health camp for socially deprived children commencing on 16 January and running for six weeks. The second involving two cases was at a 28-room elderly care facility with 21 residents and sixteen staff on the other side of the city (40 km away) from the camp. This report describes the investigations into these two outbreaks and into a possible link between them and sporadic cases elsewhere in New Zealand over a four-month period.

Methods

Outbreak 1 – health camp. A case was defined as any person who attended the camp suffering from diarrhoea of at least one day’s duration. Diarrhoea was defined as the occurrence of at least three loose stools over a 24 hour period. A shigellosis case questionnaire was administered by investigators from the PHU and included possible risk factors identified through open-ended interviews and a site visit. Cases were matched for a three day incubation period with two controls, staff with staff, children with children. Exposure to faeces was defined as physical contact with faecal matter.
All cases were asked to submit two faecal specimens. The camp swimming pool was tested for faecal indicators and the presence of Shigella species. Shigella isolates were biotyped by the Institute of Environmental Science and Research (ESR). Outbreak control measures were put in place and an environmental investigation was conducted. A multivariate analysis was conducted by conditional logistic regression using SAS software.5 Differences in attack rates and frequency of symptoms were assessed using a chi-squared test.
Outbreak 2 - rest home. A case was defined in residents and staff as in outbreak 1. Separate questionnaires were prepared and administered to staff and residents. Faecal specimens were requested and processed as in outbreak 1. An environmental inspection was undertaken.
Investigation of a possible link between outbreaks. The index cases of both outbreaks were questioned extensively to find a common source. Other notified cases of S. sonnei Biotype a gastroenteritis were investigated and laboratories were contacted to identify non-notified cases. Restriction digestion of total genomic DNA was performed using standard methods.6 Gels were run and restriction patterns were compared visually and interpreted in accordance with principles suggested by Tenover et al.7

Results

Outbreak 1 - health camp. 94 of 96 (98%) camp staff and students were interviewed. Fifteen students and fifteen staff fitted case criteria (Table 1). Nine (60%) of the students and none of the staff submitted faecal specimens within one week of illness onset; eight were positive for Shigella sonnei Biotype a. The attack rates in students (37%) and staff (28%), were not statistically different (p=0.4). The majority of students were males (68%), whereas most staff were females (79%). While 74% of the staff were Europeans, over 60% of the students were Maori or Pacific Islanders. A higher percentage of students than staff (60% versus 20%) had vomiting as part of their illness (p=0.03). The first student became unwell on the 28th of January; no staff member was unwell until over 2 weeks later (Figure 1). On follow-up at one week, only one family member of a student became unwell.
Thirteen students and 14 staff cases were matched with controls. The only variable that could be demonstrated to be associated with the risk of illness in the combined analysis (Table 2) was exposure to human faeces (OR 4.0, 95% confidence interval 1.0-16.3; p=0.05). Although ethnicity as a whole was not shown to be related to illness, there was an indication of a difference between Pacific Islanders and Europeans. For staff there was also an indication of an association of eating camp food with illness (OR 6.9, 1.0-5.0; p=0.06). One of the kitchen workers became unwell during the outbreak, but not until the 16th of February.
Problems in food inspection, storage and handling, and with wastewater discharge from the sluice were found. It was noted that the swimming pool had turned green in early February, suggesting contamination at that time. A sample of pool water as negative for Shigella spp.
Outbreak 2 - rest home. Over eleven days, four staff and four residents developed illness, with an attack rate of 24%. All were females, with an age range of 29 to 66 years for staff, and 70 to 92 years for residents. Apart from the two notified cases only one other person who had been ill had a positive faecal specimen. The median duration of symptoms was 3 ½ days (range 0.5 to 9 days). All cases, after the first one, could be explained by person to person transmission through close contact. No other risk factors were found. Opportunities for minor improvements in cleaning and disinfection were identified.
Table 1. Characteristics of those interviewed at the health camp.
Characteristic


No data
No. ill (Attack rate)
Age*
Gender (M/F)
Ethnicity
European n (%)
Maori n(%)
Pacific Island n(%)
Other n(%)
Symptoms
Duration* days
Vomiting n(%)
Diarrhoea n(%)
Other† n(%)
Student
n =43

2
15 (37%)
9 (6-12)
28/13

12 (29)
18 (42)
7 (17)
3 (7)

3 (1-12)
9 (60)
15 (100)
11(75)
Staff
n =53

0
15 (28%)
34 (14-61)
11/42

39 (74)
8 (15)
4 (8)
3 (6)

3 (1-12)
3 (20)
15 (100)
10 (67)
Total
n =96

2
30 (33%)
21 (6-61)
39/55

51 (54)
26 (26)
11 (12)
6 (6)

3 (1-12)
12 (41)
30 (100)
21 (70)
*median(range);†one or more of: fever, headache, nausea, abdominal cramps.


content01.jpg
Figure 1. Epidemic curve for health camp outbreak.

Link investigation. The index case at the health camp, an eight year old Pacific Island boy, became unwell on the evening that he returned from a weekend at home. Two other members of the household developed gastroenteritis within three days. The index case at the elderly care facility, a female resident, was cared for by a staff member who also became unwell and often purchased fruit for her. Both the boy’s mother and the staff member of the elderly care facility bought apples, packed by hand into plastic bags, from the same fruit shop in the few days before the outbreaks began. No other potential common source was identified.
Table 2. Assessment of risk factors for illness at the health camp.
Risk factor

All
Age (median/range)
Sex (M/F)
Ethnicity
European
Maori
Pacific Island
Other
School pool
Other pool
Sand pit
Human faeces
Animal faeces
Staff
Camp food
Ill (n-27)
n (%)

19 (6-61)
10/17
-
9 (33)
10 (37)
6 (22)
2 (7)
8 (30)
3 (11)
9 (33)
10 (37)
2 (7)

11 (79)
Not ill (n=54)
n (%)

15 (6-48)
25/29
-
31 (57)
16 (30)
3 (6)
4 (7)
15 (28)
4 (7)
12 (22)
6 (11)
5 (9)

11 (39)
p
Value

0.47
0.7
0.13
-
0.15
0.04
0.75
0.91
0.23
0.34
0.05
0.93

0.06
Odds Ratio
(95% CI*)

1.0 (0.9-1.1)
1.3 (0.3-5.5)
-
1.0
2.9 (0.7 –12.8)
9.0 (1.1-72.8)
1.5 (0.1 – 2.8)
0.9 (0.2-4.3)
4.2 (0.4-42.2)
2.6 (0.4-18.0)
4.0 (1.0-16.3)
0.9 (0.1-16.3)

6.9 (1.0-5.0)
*confidence interval; calculated from Odds Ratio.

During January and February, 21 people had stool specimens positive for S. sonnei Biotype a in Auckland and sixteen (76%) of these were notified. Two were flight attendants on the same flight from Samoa in early January. At least three other flight attendants on the flight had gastroenteritis. All had stayed at the same hotel. A questionnaire was circulated by mail among the flight attendants and no obvious link with outbreak 1 or 2 was established. During the period 1 January through to 30 April there were five isolates from cases of Shigella sonnei Biotype gastroenteritis in people living outside Auckland. Two of these were known to have had recent overseas travel to Samoa, and one reported staying at the implicated hotel.
The isolates of children from the health camp, flight attendants, two travellers from Samoa who returned to cities outside Auckland, and another case from outside Auckland no travel details available), were identical (Figure 2). The patterns of the isolates from residents at the elderly care facility differed by only one band suggesting that they were also the same strain.7

Discussion

We have described two geographically distinct outbreaks of Shigella sonnei Biotype a gastroenteritis that started within two days of each other. Consideration of a common exposure eventually led to a fruit shop and molecular subtyping confirmed that they were related to one another, to other cases in and outside Auckland, and ultimately to a source in Samoa. At the health camp, the inexperience of the new management, the social background of the children, and the lack of adequate hygienic measures all conspired to facilitate the propagation of the outbreak and the high attack rate among both children and staff. However, the attack rate of 24% at the elderly care facility illustrates that even when hygienic practices are relatively good, Shigella infection can spread within an institutional setting.
Exposure to human faeces as a risk factor for illness at the health camp can be interpreted as at least a marker for close contact, and eating camp food as a risk factor for staff suggests some hygienic breakdown at mealtimes. For the initial control of the health camp outbreak, several procedures were undertaken with handwashing being by far the most important of these. The role of antimicrobials in control of Shigella outbreaks is controversial, and we did not use them as a control measure. Antimicrobials are not a substitute for hygienic measures, such as hand washing with soap and water and thorough drying, in reducing the secondary spread of shigellosis. It can be argued that antimicrobials should be reserved for treatment of patients only when clinically indicated8 since this practice can lead to the development of resistant that complicate therapy.9
Figure 2. Restriction patterns for S. sonnei Biotype a isolates.

content02.jpg
Lane 1: DNA size marker. Lane 2: Child from health camp. Lane 3. Child from health camp. Lane 4: Child from health camp. Lane 5: Resident of elderly care facility. Lane 6: Resident of elderly care facility. Lane 7: DNA size marker. Lane 8: Flight attendant. Lane 9: Flight attendant. Lane 10: Recent traveller from Samoa to city outside Auckland. Lane 11: Recent traveller from Samoa to city outside Auckland (stayed at implicated hotel). Lane 12: Case from outside Auckland, travel history not known. Lane 13: Case from outside Auckland, travel history not known. Lane 14: Isolate from New Zealand reference culture collection.

Pulsed-field gel electrophoresis (PFGE) has been used to link separate restaurant outbreaks of S. sonnei infection in the United States.10 Isolates from those outbreaks had two closely related restriction patterns that differed only by a single band. The epidemiological investigation implicated parsley imported from a farm in Mexico as the source of the outbreaks. Similarly, we have used PFGE to link two geographically separate outbreaks in Auckland to a source in Samoa.
While a history of overseas travel is recorded routinely for cases of notifiable disease in New Zealand, the contribution of imported infections to the overall burden of disease and outbreaks in the country has not been quantified. Furthermore, feedback concerning imported cases to the respective public health authorities in other countries rarely occurs. The Samoan Public Health Authorities were alerted on this occasion. This particular strain entered New Zealand intermittently over at least the four months of January to April in 2001. The ongoing transmission makes it less likely that one particular person was the source, and a more fundamental problem with water supply or some other breakdown in hygiene may have occurred.
This investigation provides one example of how molecular laboratory techniques can be utilised in public health investigations. In order to take full advantage of advances in both information and molecular technology, New Zealand needs electronically transmitted direct laboratory notification of positive specimens and an expanded molecular subtyping capacity. This would lead to the identification of all specimen positive cases (only 76% were notified in Auckland) and much earlier notification, and would enable more outbreaks and the linkages between them to be identified. A model for this has been developed by Bender et al11,12 who perform routine rapid molecular subtyping of selected organisms. This model has revolutionised outbreak investigation and has been shown to be cost effective.13 This approach could be adopted in New Zealand, increasing the detection of regional and inter-regional outbreaks of infection and the identification of infectious sources.
Author Information: Philip C Hill, Public Health Physician; John Hicking, Health Protection Officer, Public Health Protection, Auckland, District Health Board, Auckland; Jennifer M Bennett, Scientist, Institute of Environmental Science and Research, Porirua; Azeem Mohammed, Health Protection Officer, Public Health Protection,Auckland District Health Board, Auckland; Joanna M Stewart, Statistician, Department of Community Health, University of Auckland; Greg Simmons, Public Health Physician, Public Health Protection, Auckland District Auckland.
Acknowledgements: We thank Basker Nadarajah and Jane Gower for their work in the investigation; Kathy Pritchard for her guidance; Dr’s Nick Jones, Lester Calder, Phyllis Taylor and Robert Scragg for expert advice.
Correspondence: Dr Greg Simmons, Public Health Protection Unit, Auckland District Health Board, Private Bag 92605, Symonds St, Auckland 1001. Fax: (09) 630 7431; email: gregs@adhb.govt.nz
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  2. Kapperud G, Rorvik LM, Hasseltveldt V et al. Outbreak of Shigella sonnei infection traced to imported iceberg lettuce. J Clin Microbiol 1995; 33: 609-14.
  3. Bruce-Coles F, Kondracki F, Gallo RJ, et al. Shigellosis outbreaks at summer camps for the mentally retarded in New York State. Am J Epidemiol 1989; 130: 966-75.
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