Interventions to Prevent and Control Food-Borne Diseases Associated with a Reduction in Traveler s Diarrhea in Tourists to Jamaica

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1 Interventions to Prevent and Control Food-Borne Diseases Associated with a Reduction in Traveler s Diarrhea in Tourists to Jamaica David V.M.Ashley, Christine Walters, Cheryl Dockery-Brown,André McNab, and Deanna E.C.Ashley Background: In 1996 a study found that approximately one in four tourists to Jamaica were affected with traveler s diarrhea (TD) during their stay. That year the Ministry of Health initiated a program for the prevention and control of TD. The aim of this ongoing program was to reduce attack rates of TD from 25% to 12% over a 5-year period by improving the environmental health and food safety standards of hotels. Methods: Hotel-based surveillance procedures for TD were implemented in sentinel hotels in Negril and Montego Bay in 1996, Ocho Rios in 1997, and Kingston in A structured program provided training and technical assistance to nurses, food and beverage staff, and environmental sanitation personnel in the implementation of Hazard Analysis Critical Control Point principles for monitoring food safety standards. The impact of interventions on TD was assessed in a survey of tourists departing from the international airport in Montego Bay in and from the international airport in Kingston in The impact of the training and technical assistance program on food safety standards and practices was assessed in hotels in Ocho Rios as of 1998 and in Kingston from Results: At the end of May 2002, TD incidence rates were 72% lower than in 1996, when the Ministry of Health initiated its program for the prevention and control of TD. Both hotel surveillance data and airport surveillance data suggest that the vast majority of travelers to Kingston and southern regions are not afflicted with TD during their stay. The training and technical assistance program improved compliance to food safety standards over time. Conclusion: Interventions to prevent and control TD in visitors to Jamaica are positively associated with a reduction in TD in the visitor population and improvements in food safety standards and practices in hotels. David V.M. Ashley, PhD, deceased July 31, 2004: formerly Health and Tourism, Ministry of Health, Kingston, Jamaica; C. Walters, MSc: biostatistician, Health Promotion and Protection Division, Ministry of Health, Kingston, Jamaica; C. Dockery-Brown, RN, MPH:TRADIJAM, Western Area Health Administration, Montego Bay, Jamaica; A. McNab: TRADIJAM, Western Area Health Administration, Montego Bay, Jamaica; D.E.C. Ashley, DM: Health Promotion and Protection Division, Ministry of Health, Kingston, Jamaica. The work was supported by the Ministry of Health, Tourism Product Development Company Ltd., and the Pan American Health Organization, Jamaica. The exit survey on tourists from Donald Sangster International Airport in 1996/7 was part of a larger study supported by SmithKline Beecham Biological (Belgium). The survey from the Norman Manley International Airport, Kingston, was jointly financed by Caribbean Action on Sustainable Tourism (CAST) of the Caribbean Epidemiology Centre (CAREC), Pan American Health Organization, and the Ministry of Health. Apart from this, the authors have no financial or other conflicts of interest to disclose. Reprint requests: Deanna E.C. Ashley, DM, Health Promotion and Protection Division, Ministry of Health, 4th Floor, 2-4 King Street, Kingston, Jamaica. J Travel Med 2004; 11: Traveler s diarrhea (TD) is the most common health problem encountered by travelers to Jamaica. A survey of 29,532 departing tourists over 16 years old conducted in found that 23.6% of tourists suffered from TD during their stay. 1 TD cases invariably occurred in outbreak clusters, 2 presumably owing to the ingestion of food or water contaminated with enteric pathogens. 3 6 While TD does not normally occur in travelers who apply the stringent rules of boil it, cook it, peel it, or forget it, it limits gastronomic experiences associated with travel to foreign countries. 7,8 It is incumbent on host countries to make sure that visitors can safely benefit from those experiences by ensuring that hotels and restaurants serving food to the population and the tourism sector, in particular, apply safe food-handling and environmental sanitation practices. 9,10 In 1996 the Ministry of Health (Jamaica) initiated a program for the prevention and control of TD. The aim of this program was to reduce attack rates of TD from 25.0 to 12.0% over a 5-year period by improving environmental health and food safety standards of hotels. Definitions of terms used throughout are presented in Table 1. 1 The aim of this article is to review data taken from several sources to assess the impact of the intervention to prevent and control TD during the period from 1996 to

2 Ashley et al, Epidemiologic Surveillance of Traveler s Diarrhea 365 Table 1 Definitions of Terms Used in This Study Traveler s diarrhea The passage of three or more unformed stools per 24 hours with at least one accompanying symptom of nausea, vomiting, abdominal cramps or pain, fever, or blood in stool 1 Attack rate (%) The proportion of departing tourists interviewed who were afflicted with traveler s diarrhea during their stay 1 Hotel incidence rates The number of persons afflicted with traveler s diarrhea relative to the occupancy of the hotel expressed as guest nights Hotel occupancy The number of guests in house per night Methods Public Health Strategy: Hotel-Based Surveillance In 1995 surveillance procedures for a select number of health conditions occurring among guests at hotels were developed and tested in 5 hotels in Negril. In 1996 they were implemented in 4 additional hotels in Negril and 11 in Montego Bay.The same procedures were introduced in 11 hotels in Ocho Rios in September 1997 and 10 hotels in Kingston and St. Andrew in May On the north coast, hotels under surveillance all had > 100 rooms, all-inclusive meal and beverage services, and monthly occupancy rates generally > 80%, subject to seasonal variations. All of the properties had a nurses station manned by trained nurses and medical doctors on call. Tourism in Kingston and neighboring regions differs in size and character. Core business is the local food and beverage trade, rather than overseas stopover visits. Only 4 of the 10 participating properties in Kingston had > 100 rooms and employed nurses. None had allinclusive meal plans. Nurses kept a logbook with brief history of all cases seen. At the end of each week, the information in the logbook was summarized according to a prescribed format and faxed to the project data management unit where the information was reviewed and processed. For the hotels in Kingston where no nurses were employed, reports were submitted by hotel health and safety committee coordinators. Data were input to an American Standard Code for Information Interchange (ASCII) file using the EPI Info program package (epidemiology program office, Centers for Disease Control and Prevention, Epi Info, Version 6.04B, 1996, Atlanta, GA, USA). Means, SDs, and frequency tables were obtained for occupancy, diarrhea cases, and accompanying symptoms. Incidence rates, hotel-specific endemic rates, and outbreaks were calculated. Intercooled Stata software (Version 7.0, Stata Corporation, College Station, TX, USA) was used to cross tabulate data by hotel, year or date,and region and test their significance by chisquared tests of association. Cuzick s nonparametric trend test was used to evaluate changes in the frequency of diarrhea occurrences through the years. 11 Food Safety and Environmental Health Standards A structured program provided training and technical assistance to nurses, food and beverage staff, and environmental sanitation personnel of selected hotels for the implementation of Hazard Analysis Critical Control Point principles for monitoring food safety standards. 12 A manual of standards and acceptable practices developed for the purpose by the Ministry of Health and Tourism Product Development Company Ltd. was used to guide the process. 13 Additional sessions sensitized hotel management to the government s proposed regulations governing tourist establishments. 14 Interim Assessment of Impact Montego Bay. An interim impact of interventions was assessed in a survey of tourists departing from the international airport in Montego Bay from December 1997 to November The data from this study were compared with a subset of the data reported by Steffen and colleagues collected in using the same questionnaire and methodology. 1 Assessment of Impact Kingston. Previous surveys have not included an estimation of TD attack rates in visitors to the south coast, who mainly use the international airport in Kingston. Surveillance of TD in this region poses different challenges because most hotels do not have nurses nor all-inclusive meal plans. Beginning in May 1999, for 1 week every month over 12 months, approximately 300 tourists and nonresident Jamaicans over 16 years of age of both sexes departing from Kingston were invited to complete a modified version of the self-administered questionnaire previously used at the international airport in Montego Bay. The questionnaire was available in English and Spanish only. Persons who were unable to understand the questionnaire, visitors who had spent more than 6 months in Jamaica, and Jamaican nationals traveling overseas were excluded. Data for the airport surveys were input to an ASCII file using the EPI Info program package and were

3 366 Journal of Travel Medicine, Volume 11, Number 6 analyzed monthly and cumulated on a quarterly and/or yearly basis. Data were cross-tabulated by year and region and their significance was assessed using chi-squared tests of association. Food safety standards. A survey of food safety hazards and risks carried out in Negril and Montego Bay during 1996 and 1997 identified the following critical control points (CCPs) at which risks for food-borne diseases were highest: (1) cleaning and sanitization, (2) temperature control of foods during pre-preparation and (cold) storage, (3) temperature control of foods during postpreparation holding and (buffet) service, (4) hand washing, and (5) solid-waste management. An assessment of standards and practices for the five CCPs was conducted by specially trained public health inspectors in Ocho Rios beginning in 1998 and in Kingston starting in For each CCP, public health inspectors recorded on standardized, precoded questionnaires, the frequency of errors of food safety practices found during their inspections, enabling the calculation of a score for each CCP, which indicated the relative compliance to recommended standards. A baseline assessment was conducted prior to the initiation of a training and technical assistance program. Reassessment of the properties was conducted annually in Ocho Rios for 2 years and in Kingston for 1 year after the program was implemented. Results Hotel Surveillance At the end of May 2002,there were 38 hotels in the surveillance network, 8,509 surveillance records, and a total of 18,591 reported diarrhea cases for a total occupancy of 20,142,945 guest nights. Incidence of TD During the period 1995 to 2002, the overall incidence of TD was significantly reduced in all regions (Figure 1). In Negril mean hotel incidence declined from cases per 10,000 guest nights to 5.54 cases per 10,000 guest nights, or by 60% (p =.01). In Montego Bay mean TD incidence rates declined from cases per 10,000 guest nights in 1996 to 3.07 cases per 10,000 guest nights in 2002,a decline of 80.9% (p =.00).In Ocho Rios the TD incidence rate declined by 77.1% from cases per 10,000 guest nights in the last quarter of 1997 to 5.31 cases per 10,000 guest nights in Finally, in Kingston the incidence of TD reported for 1999 was 1.08 cases per 10,000 guest nights. Between ,the average incidence of TD has been 0.24 per 10,000 guest nights, approximately 77.8% lower than in 1999 (p =.23). Figure 1 Incidence rates (cases per 10,000 guest nights) for traveler s diarrhea in Jamaica by region, Data were collected from sentinel hotels in various tourist regions through the hotel-based surveillance system established to monitor traveler s diarrhea and other illnesses in travelers. King = Kingston; MBay = Montego Bay; Negr = Negril; Ocho = Ocho Rios. Assessment of Impact Montego Bay. A sample of 4,122 respondents in was compared with a sample of 3,572 from the survey. The male-to-female ratio was similar in both surveys,but the mean ages of the respondents was higher in (34.55 vs yr,p =.00).There were significantly more persons on vacation (p =.00), and the proportion of visitors from the United States, the United Kingdom, and Canada was significantly higher (p =.00) during the survey. Approximately 3% more persons stayed in Montego Bay (p =.005),whereas 5% fewer persons stayed in Ocho Rios (p =.00) throughout the period of the survey. In addition, approximately 5% more persons opted for all-inclusive meal services and 4% more persons said they never ate outside of the hotel (p =.00) in the more recent survey. There was no significant difference in the mean length of stay. The cumulative attack rate was significantly lower by 24.9% in the survey period. Attack rates across the four yearly quarters ranged from 18.5 to 29.5% during the period of the earlier survey and from 17.1 to 20.2% during the period of the later survey (Figure 2). Kingston. A total of 3,617 persons of mean age years from the United States (56.6%), Canada (14.4%), and the United Kingdom (12.8%) were interviewed. They stayed on average for 9.5 days.most came for holidays,but 36.2% were in Jamaica on business. Business travelers stayed on average 4.4 days.the mean length of stay of persons with

4 Ashley et al, Epidemiologic Surveillance of Traveler s Diarrhea 367 Figure 2 Cumulative attack rates of traveler s diarrhea by yearly quarter in visitors departing via the International Airport, Montego Bay, in and Figure 3 Cumulative attack rates of traveler s diarrhea by yearly quarter in visitors departing via the International Airport, Kingston, TD was 14.6 days. The visitors stayed either with family and friends (42.6%) or in a Kingston hotel (45.4%), but 7.9% stayed in another hotel outside of Kingston. Only 3.2% and 0.7%, respectively, stayed in the hotels on the eastern and southern coasts. Of the respondents, 55.4% had all meals and drinks at their place of stay. Interestingly, close to 80% never consumed food from street vendors. The cumulative TD attack rate for the study period was 5.0%. Attack rates ranged from 9.7% during the first quarter of the study (May July 1999) to 1.7% during the third quarter (November 1999 January 2000) (Figure 3). Food Safety Standards. The assessment scores after reinspections show that the mean compliance scores for all CCPs had increased over baseline values, reflecting an overall increased compliance to public health standards (Table 2). Although these differences represented real improvements in food hygiene standards, improvements were not evenly distributed across all hotels. For example, in Ocho Rios at the end of 2 years,4 of the 11 properties failed to meet the minimum standards (score of 70) required for temperature control and hand washing, whereas in Kingston at the end of year 1,4 met minimum standards for hand washing. Only 1 of these Kingston hotels met the standard required for temperature control during pre-preparation and storage, and 2 of the 5 properties with buffet lines met the standards of postpreparation and service. Discussion Surveillance data from sentinel hotels located in the tourist resort towns of the north coast showed a decline in TD occurrences over the period of 1996 to Sentinel properties of the surveillance network accommodate approximately 80% of the tourists visiting the island. At the end of May 2002, TD incidence Table 2 Impact of Intervention on Mean Scores for Food Safety Critical Points in Ocho Rios and Kingston Hotels, Mean Scores Critical Control Point Number Assessed Cleaning and sanitization Ocho Rios Kingston 10 NE Temperature control/pre-preparation and cold storage Ocho Rios Kingston 10 NE Temperature control/postpreparation and storage Ocho Rios Kingston 10 NE Hand washing Ocho Rios Kingston 10 NE Waste management Ocho Rios Kingston 10 NE NE = no evaluation.

5 368 Journal of Travel Medicine, Volume 11, Number 6 rates were 72% lower than they were in 1996 when the Ministry of Health initiated its program for the prevention and control of TD. TD incidence declined within 2 years of initiating the program. This is confirmed by the survey of tourists who stayed on the north coast and departed from the international airport in Montego Bay. Between December 1996 and November 1998, quarterly TD attack rates declined by 24.0%. Both hotel surveillance data and airport survey data suggest that the vast majority of travelers to Kingston and the southern regions were not afflicted with TD during their stay. Since 1997, surveillance data consistently show that in every region, TD incidence rates in hotels had fallen 1 year after the program had been initiated and continued to fall until The underlying assumption was that the training and technical assistance program had improved food safety practices and standards. One year after the initiation of the training and technical assistance program, improved compliance to cleaning, sanitization, and waste management standards and practices was recorded in most of the hotels. However, standards were not achieved in the CCPs of pre-preparation and cold storage of foods, postpreparation and buffet service, and hand washing. Many reasons could account for this. The upgrading of refrigeration equipment and installation of appropriate handwashing facilities and other equipment necessitates considerable expenditure, which may not have been possible within the time frame. Second, implementation of appropriate mechanisms for monitoring and control of food preparation, cold storage, hand washing, and postpreparation activities necessitates organization, the collaboration of staff, and changes in the attitudes and behavior of workers, which requires more time. The data from Ocho Rios suggest that this can be achieved in 2 years, given the full commitment of hotel management. Hotel surveillance has provided the Ministry of Health with a sensitive public health tool for monitoring TD in Jamaica.It offers the advantage to public health of being an early warning system for outbreaks and the detection of the most severe TD cases. Additionally, it permits immediate follow-up investigations of outbreaks. Exit surveys performed in airports capture a larger cross-section of tourists and TD cases and provide reproducible data on national trends and measurement of impact. The evidence provided guidance in policy and program development. However, these surveys do not allow for quick answers and rapid responses to outbreaks. Additionally, they require dedicated staff and are expensive, which prohibits their use on a routine basis. The support of the Jamaica Hotel and Tourist Association and its regional chapters was instrumental in gaining the commitment of hotel managers and maintaining the presence of nurses in hotels. In addition to seeing patients, hotel nurses were made responsible for the surveillance of the hotel s food safety, health surveillance of staff and guests, and monitoring of environmental standards. They worked closely with chefs, food and beverage managers, and sanitation managers to implement the standards and improve worker attitudes and practices. In recognition of today s market demand for higher environmental health and food safety standards and the costs associated with TD outbreaks in hotels, health policy makers and hoteliers in Jamaica have fully committed to the wider program to improve food safety and environmental sanitation in hotels. With Jamaica s low risk for TD,its travelers will not need to take enteric vaccines or other prophylactic medications, which provide only limited protection. 1,15,16 The market advantage that this provides reinforces the commitment of hoteliers to better food safety and environmental sanitation practices. Many visitors with TD are known to take legal action to recover a ruined vacation. Using a TD attack rate of 23.6%, an average vacation stay of 7.7 days, and a mean cost of stay per day of $ (US), the loss incurred by visitors to Jamaica impaired for 10.8 hours by TD would be approximately $189,584, (US) per million visitors annually. The cost of medical care should be added to this figure. Unpublished data collected in showed that travelers to Jamaica lost vacation time at almost seven times the actual cost of a day s stay. Epidemics of TD of this magnitude could therefore cost Jamaican hoteliers up to $993,013, (US) per million visitors annually, crippling the potential for the growth of tourism in Jamaica. Currently TD incidence rates for Jamaica are probably equal to those recorded in many tourist destinations in Europe and North America that have a low risk for TD, and much lower than the rates in tourist destinations in Asia, Africa, and Latin America. 5,17 The surveillance system and the standards developed and implemented during the period of 1996 to 2000 were incorporated into regulations under the Public Health Act in 2000, 14 which will ensure that the low incidence of TD is maintained. Hotels in Jamaica are now required to submit an illness surveillance report weekly to the Public Health Department, and all require annual food safety and environmental health standards audits before they can be health certified. Acknowledgments The authors appreciate the continued support of the Jamaica Tourist Board airport interviewers; hotel managers; public health officers of the Western, North

6 Ashley et al, Epidemiologic Surveillance of Traveler s Diarrhea 369 Eastern, and Southern Area Health Authorities; data processors, Frank Chambers, Nordia Thompson, and Omar Nish; and the secretarial support of Avia McKay. The authors also thank Robert Steffen, MD (Zurich), Herbert DuPont, MD (Houston), and Nadja Tornieporth, MD (SmithKline Beecham Biologicals, Belgium), for their contributions and advice. References 1. Steffen R, Collard F, Tornieporth N, et al. Epidemiology, etiology and impact of travelers diarrhea in Jamaica. JAMA 1999; 281: Paredes P, Campbell-Forrester S, Mathewson JJ, et al. Etiology of travelers diarrhea on a Caribbean island. J Travel Med 2000; 7: Glandt M, Adachi J, Mathewson JJ, et al. Enteroaggressive Escherichia coli as a cause of travelers diarrhea: clinical response to ciprofloxacin. Clin Infect Dis 1999; 29: Gomi H, Jiang Z-D, Adachi JA, et al. In-vitro anti-microbial susceptibility testing among bacterial enteropathogens causing travelers diarrhea in four areas of the world. Antimicrob Agents Chemother 2001; 45: Jiang Z-D, Lowe B, Verenkar MP, et al. Prevalence of enteric pathogens among international travelers with diarrhea acquired in Kenya (Mombasa), India (Goa) and Jamaica (Montego Bay). J Infect Dis 2002; 185: DiCesare D, DuPont HL, Mathewson JJ, et al. A double-blind, randomized, placebo-controlled study of SP303 (Provir) in the symptomatic treatment of acute diarrhea among travelers to Jamaica and Mexico. Am J Gastroenterol 2002; 97: Kozicki M, Steffen R, Shar M. Boil it, cook it, peel it, or forget it : does this rule prevent travelers diarrhea? Int J Epidemiol 1985; 14: Mattila L, Siitonen A, Kyronseppa H, et al. Risk behavior for travelers diarrhea among Finnish travelers. J Travel Med 1995; 2: Alleyne GA. Health and tourism in the Caribbean. Bull Pan Am Health Organ 1990; 24: Thompson DT, Ashley DVM, Dockery-Brown CA, et al. Incidence of health crises in tourists visiting Jamaica, West Indies J Travel Med 2003; 10: Cuzick JA. Wilcoxon-type test for trend. Stat Med 1985; 4(1): Bryan FL. Hazard analysis critical control point approach: epidemiologic rationale and application to food service operations. J Environmental Health 1981; 44: Ashley DVM. Health and food safety manual for the hospitality industry. Kingston: Ministry of Health/Tourism Product Development Co. Ltd., Government of Jamaica.The public health act: tourist establishments regulations. The Jamaica Gazette 2000; CXXIII. Kingston: Government Printers, 2000: Svennerholm A-M, Holmgren J. Oral vaccines against cholera and enterotoxigenic E. coli diarrhea. Adv Exp Med Biol 1995; 371B: Holmgren J, Svennerholm A-M. New vaccines against bacterial enteric infections. Scand J Infect Dis 1990; 70: Von Sonnenburg F, Tornieporth N, Collard F, et al. Risk and etiology of diarrhea at various tourist destinations. Lancet 2000; 356(9224):