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Abstract

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

Background This article presents information on all potential outbreaks of infectious intestinal disease (IID) identified by Health Protection Scotland (HPS) involving residents of Scotland. Unlike other systems, this alert system covers potential outbreaks of IID rather than apparently sporadic cases and covers all gastrointestinal pathogens, all visited countries, and all groups of travelers.

Methods HPS collects information on all potential outbreaks of IID in residents of Scotland where infection is believed to have been acquired abroad and disseminates this to all public health teams in Scotland so other linked cases can be identified. Where possible HPS also disseminates the details to the national surveillance center in the country where infection is believed to have been acquired, enabling them to facilitate any investigations or control measures they believe necessary. The rate of outbreaks associated with travel to particular countries was determined using the number of visits reported for residents of Scotland from Travel Trends data from the Office of National Statistics.

Results Between 2003 and 2007, 319 such potential outbreaks were identified. Spain was the most frequently identified country reflecting the fact that it was also the most frequently visited country; the rate per 100,000 visits to Spain was 1.4, very similar to the overall rate for all countries of 1.3, while the highest rate of 46.7 per 100,000 visitors was associated with travel to Egypt. Salmonella sp was the most frequently identified pathogen within which Salmonella enteritidis was the most frequently identified serotype.

Conclusions The system provides a rapid alert mechanism for potential outbreaks of IID outside Scotland, allowing their investigation and control as appropriate and demonstrates the risks of outbreaks associated with different countries and pathogens.

Information at a national level on sporadic or apparently sporadic cases of infectious intestinal disease (IID) that are believed to have acquired their infection abroad is generally very limited. Information has sometimes been collected as part of special studies among travelers,1–6 but such information is usually restricted to particular groups of travelers, e.g., those attending travel clinics or confined to limited periods of time or particular pathogens. Limited information may also be provided on the laboratory request form that is part of the routine laboratory reporting.7 The travel details available via laboratory reports are not systematic and when provided are often just the name of the country. Many patients who are likely to have acquired their infection abroad are not reported to have done so in national surveillance, e.g., in national laboratory surveillance, approximately 1% of Campylobacter sp cases report overseas travel, while from a sentinel surveillance study, 25% of patients reported travel outside the UK.8

Most countries in Europe and North America have outbreak surveillance systems for outbreaks of either all IID or foodborne disease.7,9–11 Few capture information on outbreaks where infection is believed to have been acquired abroad.

In Scotland, Health Protection Scotland (HPS) operates a rapid alert system to identify potential outbreaks of IID in persons returning to Scotland. The identification of these potential outbreaks allows other linked cases in Scotland to be identified, and HPS to alert public health authorities in the relevant country allowing them to initiate investigations as they believe appropriate.

Methods

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

A potential outbreak of IID occurring abroad is defined as two or more confirmed cases of infection or at least one confirmed case where others are alleged to have been ill. This is a voluntary system whereby such outbreaks are usually reported by phone or e-mail to HPS by the public health teams within the 14 National Health Service (NHS) boards in Scotland, using information available on the patient’s “enteric form”. The enteric form seeks brief information about cases of IID. Its content and means of collections vary between, and sometimes within NHS boards. It is usually completed by patients either as a result of a telephone or personal interview with a member of the public health team or environmental health officer or as a postal questionnaire. Outbreaks may also, however, be identified by the reference laboratories. This is particularly the case where the detailed typing of the organism, e.g., its phage type or molecular profile is rarely seen in Scotland and/or where the individuals affected are residents in disparate regions of Scotland.

HPS’s surveillance system records from the enteric form provide a minimum data set on the potential outbreak including

  •  • 
    the organism responsible
  •  • 
    number positive
  •  • 
    number of others suspected to be affected
  •  • 
    country
  •  • 
    town/resort
  •  • 
    hotel or other accommodation
  •  • 
    catering (full board, half board, and self-catering)
  •  • 
    holiday start and end dates
  •  • 
    date of first onset
  •  • 
    tour operator
  •  • 
    flight details (if applicable)
  •  • 
    and any other relevant information.

The information is disseminated by HPS to all public health teams within the NHS boards in Scotland, so that they can identify other linked cases. Where possible information is also sent directly to the national surveillance center in the country where infection is thought to have been acquired, enabling them to facilitate any investigation or control measures they believe to be necessary. HPS communicates directly with countries within the European Centre for Disease Prevention and Control (ECDC) area and copies information to the Scottish Government. Where direct channels of communication do not exist between HPS and other national centers, HPS invites the Scottish Government to forward the information to the Department of Health International Division for them to forward to the country concerned. A copy of the information is also sent to ECDC.

This study uses data on the occurrence and characteristics of potential outbreaks from HPS’s surveillance system and compares countries using data from Travel Trends 2006, data and commentary from the International Passenger Survey.12 Using the average number of outbreaks reported per country between 2003 and 2007 and the number of visits to each country by residents of Scotland in 2006, where these data were available, we calculated the rate of outbreaks per 100,000 visits.

Results

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

The data are presented for the 5 years, 2003 to 2007 (Figure 1). During this period, HPS identified and alerted NHS boards to 319 potential outbreaks of IID in persons returning to Scotland from abroad. A total of 309/319 (97%) potential outbreaks were initially identified by the public health teams and 10/31 (3%) by the Scottish Salmonella Reference Laboratory.

image

Figure 1. Potential outbreaks of infectious intestinal disease where infection is believed to have been acquired abroad identified by Health Protection Scotland 2003 to 2007.

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All the information for the minimum data set was not available for all potential outbreaks, but information on key variables such as details of the hotel or other accommodation was high at 312/319 (98%) for the seven outbreaks where this information was unavailable and information on the town/resort was available. The holiday start date was available for 313/319 (98%) where this information was unavailable either holiday end date and/or date of onset were available. Information available on the airline and flight details was more limited, with airline only available for 54/319 (17%), but such information was always included where there was a suggestion that this could be a potential factor in the outbreak or others on the flight were ill. The nature of the other relevant information included in the alert varied between the outbreaks but included details of suspected foods or restaurants, problems with the standards of hygiene at the hotel, or use of swimming pools and water parks especially in outbreaks of Cryptosporidium sp.

The system relies on the laboratory isolation of a pathogen and the completion of an enteric questionnaire, therefore the pathogen was known for 317/319 (99%) of the potential outbreaks. There were only two potential outbreaks where the pathogen was unknown when the alert was generated. In one of these, a number of passengers became ill on the return flight, and the local public health team obtained epidemiological information from passengers once the plane landed. In the second, the public health team was alerted by a hospital of the admission of two patients who had stayed at the same hotel group in a resort.

In 10/319 (3%) potential outbreaks, more than one pathogen was identified. Salmonella sp was the most frequently identified pathogen, reported from 166/319 (52%) potential outbreaks (Figure 2).

image

Figure 2. Pathogens identified in potential outbreaks of infectious intestinal disease where infection is believed to have been acquired abroad.

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Within potential outbreaks of Salmonella sp, Salmonella enteritidis was the most frequently identified serotype in 74/166 (45%). Phage type 1 was the most commonly reported phage type among S Enteritidis, reported from 15/74 (20%), while PT21 was the second most frequent 11/74 (15%). Salmonella typhimurium accounted for only 10/166 (6%). Other serotypes, of which there were 18, caused only either one or two outbreaks each. For 62 Salmonella sp outbreaks, the typing was not available when the information was reported to HPS and circulated to all those involved in the alert system. A total of 55/166 (33%) of potential Salmonella sp outbreaks were associated with travel to Spain, 17/166 (10%) with travel to Turkey, and only 12/166 (7%) with travel to Egypt. Six of seven (86%) potential outbreaks associated with cruises were of Salmonella sp.

Among the potential outbreaks of Shigella sp, Shigella sonnei was the most frequently identified serotype accounting for 31/50 (62%). Shigella flexneri accounted for 9/50 (18%) and Shigella boydii accounted for 4/50 (8%). There was one potential outbreak of Shigella dysenteriae, one potential outbreak of Shigella sp involving two serotypes (S boydii and S flexneri), and four in which the serotype was unknown. A total of 24/50 (48%) of potential Shigella outbreaks were associated with travel to Egypt, accounting for 24/42 (57%) of all potential outbreaks associated with Egypt.

There were 23/319 (7%) potential outbreaks of verotoxigenic Escherichia coli (VTEC) infection: 21 of these were of E coli O157 and two of non-O157. A total of 7/23 (30%) potential VTEC outbreaks were associated with travel to Turkey and 4/23 (17%) with travel to Malta; these four potential outbreaks accounted for 4/6 (67%) for all potential outbreaks associated with travel to Malta. Another four potential outbreaks (17%) were associated with travel to Egypt.

There were four potential outbreaks of Vibrio cholerae and another of mixed infection of Vcholerae and Senteritidis. Three of these potential outbreaks were associated with travel to Tunisia and one each with Morocco and Mexico.

There were 51/319 (16%) potential protozoal outbreaks, 48/51 (94%) of Cryptosporidium sp and 3/51 (6%) of Giardia sp. Among the potential outbreaks of Cryptosporidium sp, 33/48 (69%) were associated with travel to Spain and 7/48 (15%) were associated with travel to Turkey.

Within the 10 potential outbreaks of mixed infection, nine involved two pathogens and one three pathogens: this was an outbreak of norovirus, Cryptosporidium sp and Shigella sonnei associated with the Dominican Republic. Salmonella sp infection occurred in 8/10 (80%) outbreaks of mixed infection.

Spain was the most frequently identified country, reported from 100/319 (31%) of the potential outbreaks; 42 (13%) potential outbreaks were associated with Egypt (Table 1). Nineteen countries were reported on just one occasion. A total of 7/319 (2%) potential outbreaks were associated with cruises. Travel within Europe was reported in 152/319 (48%) potential outbreaks: travel in Africa 82/319 (26%), Asia 56/319 (18%), North America 26/319 (8%), and South America 3/319 (1%).

Table 1.  Countries associated with potential outbreaks of infectious intestinal disease where infection was believed to have been acquired abroad
CountryPotential outbreaks
Spain100
Egypt42
Turkey33
Tunisia22
Greece14
Dominican Republic12
Morocco9
Cruise7
Bulgaria7
Mexico6
Malta6
Italy4
India4
Portugal4
Thailand4
Cyprus3
Peru3
Kenya3
Cuba3
France2
Tanzania2
South Africa2
Belgium2
Maldives2
Barbados2
Nepal2
Countries reported just once19
Total319

August was the most common month for the reporting of potential overseas outbreaks of IID to HPS, accounting for 74/319 (23%) of the annual totals. October was the second most common month, during which 46/319 (14%) potential outbreaks were reported (Figure 3).

image

Figure 3. Month in which the potential overseas outbreak of infectious intestinal disease was reported to Health Protection Scotland.

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Spain was the most frequently identified country for potential overseas outbreaks, with an average of 20 per year, but Spain was also the most frequently visited country. The rate of potential outbreaks per 100,000 visits was 1.4, very similar to the overall rate for all countries of 1.3 (Table 2).

Table 2.  Visits to countries in 2006 from Scotland and rate of potential outbreaks per 100,000 visits (for the individual countries for which data are available for number of visitors from residents of Scotland and countries with more than one overseas outbreak reported)
CountryPotential outbreaksVisits in 2006 (thousands)Rate, outbreaks per 100,000 visits
TotalAverage per year
Egypt428.41846.7
Tunisia224.41725.9
Malta61.21012.0
Turkey336.6927.2
Barbados20.666.6
Mexico61.2215.7
Bulgaria71.4393.6
India40.8302.6
Thailand40.8362.2
Greece142.81801.6
Spain1002014701.4
South Africa20.6371.1
Cyprus30.6720.8
Belgium20.6740.5
Portugal40.81610.5
Italy40.81930.4
France20.64170.1
Total all countries31963.847581.3

Egypt was the second most frequently identified country associated with potential overseas outbreaks, with an average of 8.4 per year. It is, however, much less frequently visited and the rate was consequently 46.7 per 100,000 visits, the highest rate identified with any country with more than one potential outbreak and for which travel trend data were available. The rate for Egypt was 36 times the overall rate of 1.3 per 100,000.

The second highest rate of 25.9 per 100,000 was associated with travel to Tunisia, with an average of 4.4 potential outbreaks per year.

For seven countries (Dominican Republic, Morocco, Peru, Kenya, Cuba, Tanzania, and Maldives) associated with two or more potential outbreaks, the country is not specifically identified in the travel trends data,12 and therefore, it was not possible to calculate the rate of outbreaks per 100,000 visits. Interestingly, two of these countries, Dominican Republic and Morocco, were the sixth and seventh most frequently associated countries with potential outbreaks.

Discussion

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

This system was introduced in 2000 and therefore was well established before the period of data collection reported here. The system is well supported by all the public health teams in Scotland; however, as this is a voluntary system, it is possible that a number of potential overseas outbreaks may be missed. The system may also be slightly biased by the different protocols in existence for interviewing persons with the different gastrointestinal pathogens. While it is routine practice across Scotland for all those with V  TEC infection to be interviewed, the interviewing of those with Campylobacter sp is more variable, and very few cases identified with a viral infection are interviewed and therefore there may be a greater underascertainment for some pathogens, in particular the viruses, than for others. Indeed, there were only two potential outbreaks of norovirus reported. Despite these limitations, the system provides a rapid mechanism to identify many potential overseas outbreaks, allows the identification of linked cases among other residents of Scotland, and provides information to allow the relevant public health authorities in the country involved to initiate any investigations/control measures they deem appropriate. The system covers the whole population of Scotland and is not restricted to particular high-risk groups of travelers, countries, or pathogens and therefore should be representative of all outbreaks of IID abroad involving residents of Scotland. The system is unlikely to capture those who have recovered before returning to Scotland, as it requires the patient to seek medical attention in Scotland. This helps to explain why the system detected no outbreaks of Bacillus cereus, Clostridium perfringens, or Staphylococcus aureus. Intoxication due to these pathogens tend to have a short incubation period and generally result in an illness of shorter duration than with most other gastrointestinal pathogens. Consequently, most patients will not seek medical attention when returning to Scotland. Similarly, the short duration of infection with norovirus helps to explain why relatively few such potential outbreaks were identified. The trends identified for potential outbreaks may be different from those identified for apparently sporadic cases.

Many of the potential outbreaks reported through this system are relatively small with only a few cases identified in Scotland. For many of the potential outbreaks reported to HPS, the information on the total number affected is very limited, with patients sometimes reporting that “others at the hotel were ill with similar symptoms” or “lots of others were ill” and only being able to provide details about members of their own family/travel group. However, there have also been notable examples when outbreaks that are identified initially with only a couple of cases develop into large outbreaks with cases reported from a number of other countries.

The largest outbreak identified during the period was an outbreak of Cryptosporidium sp associated with a hotel in Majorca. HPS first reported the outbreak based on one case and others alleged to be ill on July 22, 2003, with other cases rapidly identified in Scotland. The swimming pool, the suspected source of infection was closed on July 23, 2003, thereby possibly limiting the size of the outbreak.13

Another large international outbreak identified via this system was an outbreak of Salmonella Goldcoast in tourists returning from Majorca in September to October 2005. There were a total of 148 cases meeting the outbreak case definition, from around Europe, with cases identified in England & Wales, Germany, Sweden, Norway, Ireland, Denmark, Finland, Majorca, and Scotland in which there were 28 cases.14 Analysis of data from trawling questionnaires administered as part of the outbreak investigation did not generate a testable hypothesis about foods, outlets, or other potential sources of infection.

When considering the rate of potential overseas outbreaks per 100,000 visits, this is only an approximation, but allows the potential outbreaks associated with particular countries to be considered in relation to the number of visitors rather than just the total number of outbreaks per country. Another limitation was the fact that data for all countries were not available in Travel Trends.12 For example, the Dominican Republic was the sixth most frequently identified country from the overseas outbreak data with 12 potential outbreaks, but the number of visits there by residents of Scotland was not available. There was wide variation in the rates of potential overseas outbreaks per 100,000 visits ranging from 0.1 for travel to France to 46.7 for travel to Egypt. Although Spain was the most frequently reported country for potential outbreaks, the rate was 1.4, very similar to the overall rate for all potential outbreaks and overseas visits of 1.3 per 100,000, with the number of potential outbreaks associated with Spain representing the large number of visitors rather than any particular risk associated with Spain.

The high rate associated with travel to Egypt, at 36 times the overall rate, is notable. This could reflect that a greater proportion of visitors are staying in hotels where they are more likely to become aware of others being ill than in some other countries where there may be a greater proportion in individual villas where they are possibly less likely to be aware of others being ill. This would be unlikely to explain all the difference and may reflect levels of hygiene, sanitation, and prevalence of IID. The high rate of potential outbreaks is especially important as Egypt has experienced a particularly large annual growth from 2002 to 2006 in visits by UK residents, e.g., from 2005 to 2006 growth in visits was 23%.12 Therefore, there is a growing potential for more outbreaks and apparently sporadic cases of IID to be associated with travel to Egypt as visitor numbers increase.

August was the most common month for the reporting of overseas outbreaks accounting for 23% of all outbreaks. This reflects the summer holiday season and the school holidays, which in Scotland generally run from the end of June to the middle of August. Numbers remained high in the autumn reflecting people returning from summer holidays and the half-term school holiday in the middle of October.

Residents of Scotland have the potential to be part of overseas outbreaks of IID. While abroad they may be exposed to pathogens to which they have less immunity than those encountered at home. Additionally, the standards of hygiene may not be as high as in the UK, especially in some non-European countries as evident by higher rates of potential overseas outbreaks associated with some of these countries, in particular Egypt and Tunisia (Table 2). Indeed, other studies have reported risks for individuals associated with travel to Asia, Africa, and South America.1,4 Those traveling abroad need to be aware of the simple precautions they can take to reduce their chances of infection.15 In the meantime, the system provides a rapid alert mechanism for potential overseas outbreaks of IID and their investigation, although it is recognized that there are practical difficulties in the investigation of outbreaks where cases are residents in different countries and information may be limited.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

We would like to thank all the consultants in public health medicine, infection control nurses, environmental health officers, and microbiologists who contribute to the overseas outbreak system.

Declaration of Interests

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

The authors state that they have no conflicts of interest.

References

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References