Food and waterborne infections associated with package holidays

Food and waterborne infections associated with packageholidays

R.Y. CartwrightMicroDiagnostics (UK) Ltd, Merrow, Guildford

1. SUMMARY

The surveillance and prevention of food and waterborne

infections in package holiday tourists relies more on common

sense and experience rather than evidence based scientific

facts. In spite of the major economic value to both sending

and receiving countries it is a problem that is largely ignored

by health departments at both local and national levels.

Package holiday tourism is a growing industry with over

20 million holidays sold every year in the UK. Destinations

are in every continent including countries with poorly

developed, as well as those with an advanced, public health

infrastructure. The incidence of gastrointestinal infection is

not reflected in official surveillance programmes as they

largely fail to capture information on travel associated

infections. Outbreaks of food and waterborne infections in

these resorts are largely not investigated. Major British tour

operators have responded by developing a crude but

effective continuous surveillance system for subjective

travellers’ diarrhoea.

The importance of food and water hygiene is, however,

not ignored and proactive preventative programmes are

being developed and implemented in some resort as well as

by the tourist industry and international agencies. There is a

need for further cooperation and partnership between

workers in different countries, different disciplines and

between the public and private sectors.

2. INTRODUCTION

International tourism is growing rapidly with an estimated

increase in 2000 of 7Æ4% bringing the total number of

international arrivals to 699 million according to the World

Tourism Organisation (2001). Europe accounts for 58% of

international tourism with 403 million arrivals in 2000. In

the UK about 50% of holidays are taken as packages that

include transport and accommodation. The UK package

holiday market has increased with sales increasing from

10Æ66 million package holidays in 1986 to 20Æ03 million in

2000. Over 90% of package holidays sold in Britain are

provided by a few major operators who together comprise

the Federation of Tour Operators (FTO). The number of

destinations increases annually. In 2001, one of the larger

operators provided holidays in 33 different countries using,

in the summer season, over 1400 different units of

accommodation.

A study of infectious intestinal disease (IID) in England

by the Food Standards Agency (2000) estimated that 20% of

the population suffered an IID in a year. Travel abroad

generally was associated with an increase in IID and

although no difference was observed in those travelling to

northern Europe, the risk to those visiting southern Europe,

Mediterranean countries and the Middle East was interme-

diate and, for travel to other countries, was large.

Surveys of illnesses in returning package holiday tourists

were undertaken at airports around 1980. Reid et al. (1980)

reported that for tourists returning to Glasgow, gastroin-

testinal upsets were the most frequent holiday associated

1. Summary, 12S

2. Introduction, 12S

3. Food and waterborne infections, 13S

4. Surveillance and investigation, 14S

4.1 Formal systems, 14S

4.2 Tour operator surveillance using the consumer

satisfaction questionnaire, 15S

4.3 Tour operator surveillance - resort staff records, 16S

4.4 Consumer groups, 17S

5. Investigations, 17S

6. Examples of incidents and situations, 18S

6.1 1984 Albufeira, Portugal, 18S

6.2 1989 Salou, Spain, 19S

6.3 1997 Portinatx, Ibiza, 20S

6.4 1990–2000 Dominican Republic, 20S

6.5 1991 Salmonella in flight meals, 21S

6.6 Emerging pathogens in package tourism, 22S

7. Discussion, 23S

8. References, 24S

Correspondence to: R.Y. Cartwright, MicroDiagnostics (UK) Ltd, 55 Holford

Road, Merrow, Guildford, GU1 2QE (e-mail: [email protected]).

ª 2003 The Society for Applied Microbiology

Journal of Applied Microbiology 2003, 94, 12S–24S

illness and that the incidence was highest in those who had

visited North Africa. Steffen et al. (1983) reported similar

findings in a survey of 16 568 travellers returning on charter

flights to Switzerland and Germany. Neither of these studies

identified the cause of the gastrointestinal upset, only

recording symptoms.

A search of records available from national surveillance

centres produces very little information on travel associated

infections, with the exception of a few specific pathogens

and even then it is a record of the number of cases reported

with no information on the number of travellers. The

Communicable Disease Report from the Public Health

Laboratory Service of England and Wales has a regular

section on common imported diseases but this primarily

relates to a few viruses and parasites. It does not provide any

meaningful information on travel-associated infections.

In spite of this, the majority of travellers and medical

practitioners can easily list a number of countries associated

with travellers’ diarrhoea under one of its many synonyms.

‘Dehli Belly’ and India, ‘Montezuma’s Revenge’ and

Mexico, ‘Tunisian Two Step’ and Tunisia, ‘Pharaoh’s

Curse’ and Egypt to name but a few of the descriptive

terms and the associated countries. Experienced travellers

are well aware that travel to most tropical and subtropical

countries, especially those with a developing public health

infrastructure, requires special care in what food and drink

is consumed. Even with precautions, however, consumer

organization publications such as Holiday which report

high levels of stomach associated illness in travellers visiting

these destinations (Consumers Association 1999).

Travellers’ diarrhoea can be caused by a wide range of

gastrointestinal pathogens and have been the subject of

reviews including those by Farthing (1992), Cartwright

(1993), Castelli and Carosi (1995), and Cartwright and

Chahed (1997). A study by Steffen et al. (1999) in Jamaica

revealed that the most frequently detected pathogens were

enterotoxigenic Escherichia coli, Rotavirus and Salmonella

species.

The source of the pathogens causing travellers’ diarrhoea

has been largely conjecture but it generally assumed that the

predominant route of spread is through contaminated food

or water. In addition to the background of travellers

diarrhoea, ‘classical outbreaks’ of foodborne and waterborne

infections affect package tourists and, although they may

attract considerable media attention, they form a relatively

small part of the overall disease burden.

The control of food and waterborne infections is the

responsibility of public health authorities. Most countries

have legislation regarding food and water hygiene, but the

implementation of the law varies with, very understandably,

public health priorities being focussed on diseases such as

Acquired Immunodeficiency Syndrome and tuberculosis. In

this context it should also be remembered that the majority

of food and waterborne infections in tourists do not impinge

on the health services of holiday countries. The illnesses can

usually be controlled by self-medication, or medical assist-

ance postponed until the tourist returns home. The resort

public health authorities may be unaware of problems and

only hear about them at a later date through international

reporting.

This review considers some aspects of the work under-

taken by major British tour operators over the past 20 years

to reduce the incidence of food and water associated

infections in package tourists. They do not have the

advantage of teams of epidemiologists and microbiologists,

nor do they have the authority to investigate outbreaks.

Cooperation with local public health authorities has been

mixed and frequently it has been more effective to work

through Ministries of Tourism rather than Ministries of

Health. It has become apparent that the control of food and

waterborne infections is best achieved in many countries

through a multidisciplinary approach.

The UK operators have developed a crude but useful

surveillance tool that has, for over 20 years, provided

continuous monitoring of the incidence of stomach related

upsets associated with the majority of resorts used by UK

package tourists. There have been few formal investigations

of outbreaks, incidents or high background illness levels and

consequently most information is descriptive and subjective.

It has, however, been sufficient to stimulate improvement

programmes resulting in major reductions in the incidence

of gastrointestinal upsets among package tourists. These

programmes have also been considered as beneficial to the

health of the local indigenous population. It has been a

salutary reminder that many of the major improvements in

public health hygiene in the UK occurred before there was

any knowledge of the microbes responsible for the cause of

gastrointestinal diseases.

Although the situation is far from satisfactory, especially

for the package holiday tourist, it should be recognized that

many tourists do not use a package and they are potentially

at greater risk as they may use accommodation and eating

establishments whose standards are not influenced by tour

operators.

3. FOOD AND WATERBORNE INFECTIONS

The spectrum of food and waterborne infections is wide

including cholera, campylobacteriosis, cryptosporidiosis,

E. coli infections, salmonellosis, shigellosis, enteric fevers,

brucellosis, hepatitis A, amoebiasis and trematode infections.

Legionellosis is also waterborne. This review concentrates on

those infections that result in a gastrointestinal upset and as

such also fit the diagnosis of travellers’ diarrhoea.

A causative pathogen is isolated from very few package

tourists and then it is only as a result of the tourists visiting

HOLIDAY FOOD AND WATER INFECTIONS 13S

ª 2003 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement, 94, 12S–24S

their own general practitioner who arranges for a faecal

examination. In a few resorts if a tourist is admitted to a

local clinic, a laboratory confirmed diagnosis might be made.

It is extremely rare for any food or water microbiology

aimed at identifying a pathogen to be undertaken. Similarly

epidemiological investigations in resorts are uncommon.

The result is that, although food or water may be considered

the probable source of some infections, the proof that would

be normally expected in the UK is lacking (CDSC 1991).

The tourist industry has recognized this problem and,

rather than relying solely on definitive diagnoses and source

identification before taking any action, respond to sympto-

matic reports from tourists. As a rule of thumb, a stomach

upset lasting more than 24 h in a tourist is termed subjective

travellers’ diarrhoea (STD) and is used as an indicator of

possible food or waterborne disease.

Within the overall category of gastrointestinal illness in

tourists a number of distinct different illness categories are

recognized. The commonest is characterized by diarrhoea

with nausea and some vomiting that commences during the

first few days after arrival in a resort and generally lasts

2–3 days. This is classical travellers’ diarrhoea, with entero-

toxigenic E. coli the most frequently identified pathogen. If the

illness lasts 18–36 h and is characterized by vomiting with

some diarrhoea with the onset at any time during the holiday,

the causative agent is commonly the Norovirus. Although

Norovirus infections may be associated with the consumption

of contaminated water or shellfish, the virus may be readily

spread through the air and the environment. Less frequently,

but nevertheless with significant frequency, cases and some-

times outbreaks of the classical forms of gastroenteritis are

reported. The signs and symptoms of salmonellosis, shigel-

losis, giardiasis, E. coli O157 infection, campylobacteriosis and

cryptosporidiosis are the same whether the infection occurs at

home or on holiday.

4. SURVEILLANCE AND INVESTIGATION

The surveillance of food and waterborne infections in

package tourists has not only relied on the formal systems,

but alternative and complimentary systems have also been

developed. These have assisted in recognizing both out-

breaks and deficiencies in the public health infrastructure of

some destinations.

The investigation of outbreaks and high background levels

of gastrointestinal illness in tourists is variable with little

formal action being taken in most resorts.

4.1 Formal systems

In many countries the surveillance systems for the detection

and reporting of infections, including water and foodborne

diseases, are weak or non-existent. Resources for investigation

purposes are meagre and public health priorities are targeted

at disease that impact more directly on the health and economy

of the country. This situation is compounded by the lack

of accredited laboratories that are adequately funded and

staffed to undertake relevant microbiological investigations.

Even in countries with a well-developed surveillance and

health infrastructure data collection on travel-associated

infections is inadequate. Illnesses in package tourists that are

contained within the holiday country are very rarely notified

to the authorities in that country. Even when significantly

large outbreaks have occurred there may be considerable

pressure from hoteliers to prevent any formal notification as

‘this may be bad for business’. Even if notification does occur

local political pressures may prevent any further action being

taken.

The surveillance of communicable diseases in the UK is

well developed and, although information on travel-associ-

ated illnesses is very deficient, it has enabled outbreaks

caused by specific pathogens to be identified. It should be

remembered, however, that the system depends on tourists

consulting their general practitioner, a faecal specimen being

submitted to a laboratory, a pathogen being isolated or

identified and the result being reported to the Public Health

Laboratory Service (PHLS), Communicable Disease Sur-

veillance Centre (CDSC), or in Scotland to the Scottish

Centre for Infection and Environmental Health, together

with the travel information. The number of cases being

reported compared with the number of those infected is

likely to be low and the lack of information on the number of

tourists visiting a suspect source destination means that the

incidence of disease cannot be determined.

Information from CDSC is, however, shared with Enter-

net, the international surveillance network for Salmonellae

and E. coli, and also transmitted, as appropriate, to the

regional office of the World Health Organisation and the

Ministry of Health of the holiday country. This whole

procedure may take weeks, or even months, so that local

investigations, even if possible, may no longer be relevant.

No information is available on the incidence of package travel

associated illness from established surveillance systems.

Formal systems do, however, identify cases of specific

infections that may be of great public health importance, not

only for tourists but also the indigenous population of the

country concerned. The enteric fevers because of Salmonella

typhi and Salmonella paratyphi are recognized as important,

although infrequent, causes of food and water associated

infections in package tourists. The potential seriousness of

these infections has led to formal investigations in the

countries concerned. More recently reported cases of E. coli

O157 have received particular attention.

The transfer of information from holiday countries of

illness outbreaks in tourists to the governments of sending

countries and to the tour operators is lacking.

14S R.Y. CARTWRIGHT


4.2 Tour operator surveillance using theconsumer satisfaction questionnaire

In the 1980s it was generally recognized in the tourist

industry that certain destinations were associated with an

above average incidence of gastrointestinal illnesses in

package holiday tourists. There was, however, no measure

of the levels of illness in resorts, reliance being placed on the

impressions of staff in resort and the number of complaints

from returning tourists. Representations to government

officials in high incidence areas were usually countered with

the comment that there was no proof and it was just the

English who complained.

Major tour operators collected a considerable amount of

information for marketing purposes from returning tourists

by means of a client satisfaction questionnaire (CSQ)

completed by adult tourists during the return charter flights

to the UK. The CSQs primarily collected information that

would be of use to the operators in designing their

programmes for future seasons. As CSQs were issued on

every flight it gave a continuous stream of information

enabling trends over time to be observed as well as

differences between resorts.

A suggestion that a health questionnaire be included was

met with opposition from the tour operator’s legal advisers

who feared that attention might be drawn to illnesses with a

subsequent increase in demand for compensation. Eventu-

ally it was agreed to insert a question asking if the tourists

had been ill during their holiday and if so with what illness.

The illness descriptions were categorized, according to laid

down criteria, by the clerks entering data from the CSQs

into a computer. The term STD was coined for illnesses

described as a stomach upset, diarrhoea or vomiting.

In the first few years, only a sample of the CSQs were

analysed according to the commercial requirements of the

operator, the proportions varying between resorts. Never-

theless, the total number of CSQs analysed each year

exceeded 200 000. The data was analysed monthly using the

statistical analysis system SPSS. The standard output

chosen gave the monthly incidence of STD for each holiday

region and resort. Further analysis could be undertaken to

hotel level but the numbers were often too small to enable

any meaningful statistics to be obtained.

In 1995, the health question was refined initially to ask

specifically if during their holiday they had suffered from a

stomach upset and data entry using optical mark readers was

introduced. In the same year the annual number of

questionnaires analysed exceeded 1Æ5 million.

In summer 2000, the question was further refined to ask if

any stomach upset lasted for more than 24 h. The purpose

of this refinement was to reduce the number of reported

stomach upsets following an episode of excessive alcohol

intake.

As of 2002, further tour operators have included the latest

question in their CSQs and it is expected that upwards of

3–4 million sets of data will become available for analysis.

The analysis results are produced monthly and as such are

retrospective.

Although the change in the questions prevents a com-

parative longitudinal analysis to be undertaken, over the

years the pattern of illness between geographical areas for

each year is remarkably similar.

It was recognized from the outset that such information

was very crude in formal surveillance terms and was in no

way controlled or substantiated. The data was also restricted

to tourists over 16 years of age. The question was whether

the information provided would be sufficient for the purpose

for which it was required. The requirements were to identify

problem areas, to work with local authorities and hoteliers in

identifying causes, to take remedial actions and to assess the

effectiveness of such actions.

It rapidly became apparent that suspect problem areas

were indeed those with a higher level of travellers’ diarrhoea

and that some resorts previously not suspected warranted

closer inspection.

The number and location of resorts and hotels is variable

both between summer and winter seasons and from year to

year as the operators develop their programmes. Popular

destinations have, however, remained relatively constant

over the 20 years that this surveillance method has been in

operation. Southern European and Mediterranean destina-

tions take the majority of package holidaymakers, but there

has been a growing number of long haul destinations in

Africa, Asia, America and the Caribbean. In summer 2001, a

total of over 1 million CSQs were analysed with tourists

visiting over 500 resorts in 33 countries and staying in over

2000 different hotels.

As the make up of destinations is very different between

winter and summer seasons, with family holiday seaside

resorts predominating in the summer, and ski and long haul

sunspots in the winter seasons, the seasons are analysed

separately.

A major drawback of this form of surveillance is that it

provides no information, either microbiological or epidemi-

ological, as to the cause of the illnesses. It does, however,

provide an indicator as to where further studies may be of

value and also, because of the ongoing nature of the study,

does provide a measure to assess the effectiveness of any

remedial measures.

Geographical variations The overall geographical pattern

of STD has altered little over the past 13 years. Compared

with southern European destinations, the north African,

Caribbean and Central American destinations were associ-

ated with an appreciably higher level of stomach upsets.

(Table 1).



This information compares well with the anecdotal

information and the results of the airport passenger surveys

and demonstrates that between 1989 and 2001 the areas of

higher risk remain unaltered.

In summer 2001, of 709 579 UK tourists completing

CSQs 6% recorded a stomach upset lasting more than 24 h.

In those returning from Switzerland the incidence was 2Æ5%

while those returning from Egypt it was 30Æ8% (Fig. 1).

This higher rate has been relatively unaltered for many

years.

When the regional results are further examined by resort

it is possible to ascertain whether any problems are restricted

to a smaller geographical area or whether there is a larger

problem that may reflect the state of the public health

infrastructure. Resort data similarly can be examined to

hotel level providing information that may suggest a food

hygiene problem within one hotel or a community wide

situation that may indicate, for example, a water supply

problem.

An example of this examination of regional results for

Tunisia is given in Table 2. In 1989 here was an overall

STD incidence of 17% in 3949 tourists. In 2001, the overall

incidence was 21% in 11 149 tourists.

There is an overall similarity in the levels and patterns of

illness for each resort, and in both 1989 and 2001. The actual

questions asked varied, as in 1989 the tourists stated their

illness whereas in 2001 they were asked if they had a

stomach upset lasting more than 24 h. The hotels used in

the 2 years also were different as some were dropped from

the programme and others added but with little overall

effect on the incidence. The breakdown for the resort of

Monastir (Table 3) shows an overall similarity between

hotels in 1989 with no single hotel being responsible for the

overall level of illness. The incident values for some hotels

have no significance due the small denominator. In 2001,

hotel 5 from 1989 was the only one remaining in the

programme. The seasonal incidence of STD was 21% in

1989 and 22% in 2001. Similar findings have been observed

in other years and can be interpreted as reflecting the overall

state of hygiene and environmental control in the country,

coupled with the level of the public health infrastructure.

This is supported by little observed change in illness levels

in spite of the introduction of intensive food hygiene

programmes in hotels by the Tunisian government.

In 1997, there was a Salmonella outbreak associated with a

hotel in Ibiza. In Table 4 the monthly CSQ incidence

pattern of resort 3 differs from the other two resorts with an

increase in June. Analysis of the hotel associated illness for

this resort indicated that the problem was associated with

hotel 3. The pattern of illness coincided with an outbreak of

Salmonella food poisoning in this hotel. The CSQ results

also indicate that the outbreak was successfully controlled.

4.3 Tour operator surveillance – resort staffrecords

Neither formal surveillance nor the tour operator CSQs

provide immediate information on a situation of food or

waterborne illness as it occurs. If immediate action is to be

taken to control an outbreak, prompt notification is neces-

sary. When a tourist in a package becomes unwell the usual

response is to try self-medication then, if that is not

effective, to inform the tour operator representative. There

is a general reluctance by tourists to seek medical assistance

in another country unless absolutely necessary. It has proved

very difficult to arrange with tour operators for the

representatives to keep records of reported illnesses, but a

system is being introduced to record basic information. The

provision of early information on outbreaks together with

clinical information, even if very basic, is of great value in

EgyptDominican Republic

MexicoTunisia

CubaTurkey

St LuciaJamaicaAntigua

BarbadosZakynthos

Costa DoradaMalta

MajorcaCyprus

Costa BravaGran Canaria

TenerifeNeopolitan Riviera

Greek MainlandCorfu

AlgarveRhodes

CreteMinorcaFloridaAustria

Switzerland

0 10 20 30

Incidence (%) of subjective travellers' diarrhoea

Fig. 1 Incidence of subjective travellers’ diarrhoea in British package

holiday tourists summer 2001

Table 1 Comparative incidence of subjective travellers’ diarrhoea of

different destinations compared with Majorca

Region 1989 1993 1998 2001

Spain – Majorca 1 1 1 1

Spain – Costa Brava 1 1Æ1 1Æ2 1

Spain – Costa Dorada 1Æ7 1Æ3 1Æ1 1Æ1Portugal – Algarve 1Æ6 1Æ2 1Æ1 0Æ8Greece – Zakynthos 1Æ2 1Æ8 1Æ7 1Æ2Malta 1Æ2 1Æ3 0Æ8 1Æ2Turkey 5Æ5 5 3 3

Tunisia 4Æ4 5Æ2 3 4Æ2Egypt Not used 8Æ4 3Æ7 6Æ2Dominican Republic Not used 9Æ1 3Æ2 6

Mexico 7Æ4 5Æ2 4Æ1 4

Florida 0Æ4 0Æ6 0Æ8 0Æ6

16S R.Y. CARTWRIGHT


assessing whether they are likely to be because of bacterial

food poisoning or because of the Norovirus. The distinction

is important, as it will affect the subsequent actions that

need to be taken.

4.4 Consumer groups

Increasingly tourists consumer groups are collecting infor-

mation from disgruntled tourists who have been affected by a

gastrointestinal upset on holiday. The information will

frequently include the results of any laboratory tests arranged

by the tourist’s general practitioner. The consumer groups

tend to contact the relevant tour operator demanding that

action be taken. This system has on occasions provided the

earliest notification of a problem, as formal reporting of

laboratory results may take a week or more. The first

indication of a major swimming pool associated outbreak of

cryptosporidiosis in 2000 in Majorca was by this means. At

present a drawback of consumer group notification is that it is

usually not possible to obtain confirmation of the results or to

obtain further details of the travel. Reporting by this route is

also frequently followed by litigation with the provision of

further information being moderated by lawyers.

5. INVESTIGATIONS

Formal investigations are rarely undertaken or, if they have

been, the reports are not generally available. Such investi-

gations would normally be the responsibility of the local

public health departments who do not usually receive any

substantiated information on an outbreak at an early time

enough to undertake a meaningful investigation. The

resources available are also frequently minimal, with the

investigation of outbreaks in tourists being low in their

priority order. Staff from CDSC have given advice on

outbreak investigation but they have no authority to

Table 2 Incidence of subjective travellers’ diarrhoea in British package tourist visiting Tunisia in summers 1989 and 2001

May June July August Sept Oct Total season

Resort 1989 2001 1989 2001 1989 2001 1989 2001 1989 2001 1989 2001 1989 2001

Hammamet 11 9 13 10 19 16 30 24 28 27 15 24 18 18

Monastir 18 12 17 16 16 36 20 29 20 22 23 15 18 23

Port El Kantaoui 16 7 15 12 18 22 14 27 24 25 6 26 15 21

Sousse 10 11 19 17 17 28 18 27 23 27 9 27 16 23

Tunisia – all resorts 13 9 16 14 18 24 23 27 25 25 15 25 17 21

Table 3 Subjective travellers’ diarrhoea associated with hotels in Monastir, Tunisia in summer 1989

May June July Aug Sept Oct Total season

Hotel % n % n % n % n % n % n % n

1 18 45 7 14 14 14 24 17 31 13 20 10 18 119

2 25 16 21 19 7 15 17 36 21 28 60 5 20 119

3 17 6 0 0 0 4 19 26 14 36 11 19 13 104

4 14 22 22 27 23 22 29 17 11 36 11 9 18 134

5 18 39 18 17 21 14 28 18 31 32 28 18 21 171

Monastir all hotels 18 128 17 83 16 69 20 130 20 145 23 62 18 670

%, Incidence; n, number of CSQs in analysis.

Table 4 Incidence of subjective travellers’

diarrhoea associated with Ibiza, three resorts

on the island and three hotels in resort 2, 1997

May June July Aug Sep Oct Season

Ibiza 11 12 15 14 13 12 13

Resort 1 12 11 16 12 15 13 13

Resort 2 10 11 16 14 13 14 13

Resort 3 10 17 20 16 13 10 15

Hotel 1 10 16 13 19 16 9 14

Hotel 2 2 8 2 15 3 0 5

Hotel 3 7 23 36 12 8 7 19



undertake investigations in another country unless formally

invited by the government of that country.

The Catalan Public Health Department investigated an

outbreak of typhoid fever in Salou, Spain in 1989 with

invited support from the PHLS and, in 1999, a suspected

outbreak of paratyphoid B in Antalya, Turkey was inves-

tigated by a joint European team coordinated by staff from

CDSC but facilitated by the FTO.

An outbreak of gastroenteritis on a cruise ship in the

Mediterranean was investigated by a team from CDSC at

the request of, and financed by, the tourist industry

(McEvoy 1996). This ship outbreak could be investigated

as the vessel was in international waters.

A questionnaire study into Norovirus-like illness in

Andorra in February 2002 was undertaken in Eire and

Northern Ireland as substantial illness in passengers of

returning flight to Dublin and Belfast was reported to the

port health authorities (Feely and McKeown 2002).

The major UK tour operators are not in a position to

undertake outbreak investigations, yet they have a legal

responsibility to ensure that their clients are not unneces-

sarily put at risk. In the event of a suspected outbreak of

foodborne infection they usually send an independent

consultant to the hotel or hotels concerned to undertake a

risk assessment and to make any necessary recommenda-

tions. The consultants have trained as environmental health

officers, many reaching senior positions in local authorities,

before joining a consultative company. These consultants

can only work within the hotels with the agreement of the

manager. An inspection of the kitchen and food hygiene

practices is undertaken, and the quality of the water in the

hotel checked. Increasingly it is the policy to liase with the

resort public health department to share information. As

such a consultant’s inspection is not an outbreak investiga-

tion but may identify possible causative factors that can be

remedied. This is a reflection on the practical problems in

dealing with possible food and waterborne infections in

package holiday tourists. Local authorities will not usually

consider an investigation as a matter or priority, whereas the

tour operator will be mindful that at all times there will be

aircraft in the air bringing new tourists to a destination.

Every effort must be taken to ensure their safety.

6. EXAMPLES OF INCIDENTS ANDSITUATIONS

This section provides examples of some outbreaks and

situations of possible food or waterborne infections that have

occurred between 1984 and 2000.

6.1 1984 Albufeira, Portugal

In August, an increasing number of tourists reported

gastroenteritis characterized by diarrhoea, abdominal

cramps and nausea to their tour operator. Guests in hotels

in different parts of the town were affected with attack rates

of up to 85%.

The results of a questionnaire survey of returning tourists

from this and an adjacent resort confirmed that in late

August over 65% of tourists to Albufeira had gastroenteritis

compared with 39% in a neighbouring resort. Samples of

water from the public water supply revealed the presence of

coliforms.

Reports were being received by CDSC and Scandinavian

surveillance centres of an increase in the number of

gastrointestinal pathogens from tourists returning from

Albufeira. The predominant isolate was Shigella sonnei,although Salmonella spp, Campylobacter and Giardia lamblia

were also reported.

The attendance record at the local health clinic showed

that in early August there was a distinct rise in the number

of cases presenting with diarrhoea (Fig. 2). Those affected

were the indigenous population, Portuguese tourists and

foreign tourists.

The pattern of illness throughout the community sugges-

ted the possibility of contaminated water. The water supply

system was investigated by the Algarve Public Health

Department together with invited assistance from the

PHLS. Major deficiencies were identified with totally

inadequate chlorination of the water supply. Inadequacies

1 11 21 31 10 20 30 9 19 29 9 19 29 0

20

40

60

80

100

Pat

ient

s w

ith d

iarr

hoea

August September OctoberJulyFig. 2 Patients with diarrhoea attending the

clinic in Albufeira 1984

18S R.Y. CARTWRIGHT


in the sewage disposal system were also identified with raw

sewage passing over the beaches used by tourists.

In view of the severity of the situation emergency

chlorination of the water supply was undertaken by adding

bleach to all the service reservoirs. Over the subsequent

months major works were instituted to ensure the safety of

the drinking water supply and to bring the sewage system

and treatment works up to an acceptable standard. The level

of gastrointestinal illness fell after chlorination of the water

supply, and the level of STD fell from a peak of 50% in

1984 to under 20% in subsequent years.

Although not proven, there is strong suggestive evidence

that the gastroenteritis was associated with both drinking

and recreational waters. The outbreak was investigated by a

joint Portuguese British team led by the Medical Officer for

Health of the Algarve. Major expenditure was necessary to

improve the public health infrastructure but was beneficial

to the indigenous population as well as the tourists.

6.2 1989 Salou, Spain

In mid-July, a tour operator became aware of an unexpected

increase in reports of diarrhoea and vomiting among their

clients. Eleven tourists had been admitted to the local clinic

requiring rehydration. The local authority was aware of the

problem and had tested foods and water samples although

the results were not known. Shortly afterwards three cases of

typhoid fever in tourists recently returned from Salou were

received by CDSC. A resort visit was made by a medical

consultant on behalf of the tour operator to investigate the

high level of gastroenteritis. It was observed that the tap

water had a very high saline content and was undrinkable.

Hotels were obtaining water from lorries, the source of the

water not being known.

Following the typhoid reports an investigation was

undertaken by the Catalan Public Health Department with

invited assistance from the PHLS.

A total of 15 cases of typhoid fever were reported from

returning tourists from Salou and the neighbouring Cam-

brils; seven from England and Wales, two from Switzerland,

one from each of Sweden, Eire and Spain, in addition to

three local inhabitants. Twelve of the isolates were typed at

the PHLS Central Public Health Laboratory in London.

Three different phage types were recognized. Nine were

type A, two were type C1 and one was type E1. The cases

had stayed at different hotels or lived in different parts of

the municipalities and no common feature such as eating at a

restaurant or bathing from the same beach could be

identified.

Hotel kitchens were inspected and food handlers screened

for Salm. typhi. No carriers were identified.

Most hotels were obtaining water from lorries that had

been filled from various inland wells and rivers, some of

which were unlicensed. The inadequacy of the public water

supply had been recognized as a result of the wells becoming

exhausted and the saline content of the water rising. A new

public water supply had been constructed with a river source

and fortuitously was due to become operational within a few

weeks.

It was considered that contaminated lorry water was the

most probable source of the infections. The multiple phage

types indicated sewage contamination of the water from a

community or communities containing a number of typhoid

excretors. Hoteliers were given advice on the importance of

only purchasing water from approved suppliers and on the

management of the water within their buildings. The new

public water supply became operational within a few weeks

of the outbreak and this was accompanied by a sharp drop in

the number of cases of gastroenteritis and no further cases of

typhoid fever.

The CSQ results revealed that there had been a high

incidence of STD the previous year but this had not been

accompanied by any reported typhoid fever cases. The

following years, after the new water supply became opera-

tional, the incidence of STD was greatly reduced (Fig. 3).

Although there was a general improvement in hygiene

standards, it is most probable that the reduction in

gastrointestinal illness was associated with the introduction

of the new water supply. The typhoid outbreak, while not

proven, was also most probably waterborne.

This outbreak underlies the importance of adequate

drinking water supplies and the problems that can be

associated with unofficial supplies. Although the presence

of S. typhi was not demonstrated in lorry water supplies

the circumstantial evidence is very suggestive. It was

fortunate that the new public water supply became

operational within such a short time. The publicity

surrounding this outbreak severely affected the number

of tourists visiting the resort in the subsequent years

m j j a s o m j j a s o m j j a s o m j j a s o0

5

10

15

20

25

30

Sub

ject

ive

trav

elle

rs' d

iarr

hoea

(%

) New water supply

1988 1989 1990 1991

Fig. 3 Subjective travellers’ diarrhoea in British tourists visiting

Salou, Spain 1988–1991



underlying the fact that food and waterborne infections can

have major economic consequences.

6.3 1997 Portinatx, Ibiza

In mid-June, there was a sudden increase in the number of

guests in one hotel reporting with diarrhoea and vomiting. In

the following week, cases of Salmonella enteritidis phage type 8

infections were reported to CDSC. In the period 20–29 June,

92 illness reports were recorded by the representative of the

tour operator in the hotel, from 17 of these S. enteritidis phage

type 8 was isolated. In mid-July a further 73 illness cases were

recorded, with S. enteritidis phage type 8 being isolated from

17 of these cases.

The local health department was notified of the findings

but no formal investigation was undertaken. The tour

operator arranged for hygiene consultants to visit the hotel

and inspect the kitchens and food handling practices. Major

deficits were observed with no adequate separation of raw

and prepared foods, slicing machines being used for raw and

cooked foods with insufficient cleaning, poor refrigeration

facilities and a lack of understanding of food hygiene

principles by the senior kitchen staff. It was not possible to

arrange any bacteriological examination of foods or the

environment. It was observed that the only poultry used in

the kitchen was turkey. This was on the menu twice every

week. It was purchased as frozen 5 kg rolls that were

thawed, but the inner temperatures not checked, before

cooking. The turkey originated in France being driven to

Barcelona then shipped to Ibiza. The local public health

department had no information on the bacteriological

quality of this product and were unwilling to undertake

any testing.

A thorough cleaning programme was introduced and a

trainer chef installed to take over the food preparation and

train the staff in the kitchen. All turkey rolls were cut in half

for thawing and cooking not commenced until the core

temperature was above 4�C. The core cooking temperature

reached at least 80�C. Medium- and long-term plans to

improve the kitchen facilities were drawn up. It was decided

not to withdraw guests from the hotel as the new chef was of

the opinion that safe food could be produced from the

kitchen with proper supervision. No further cases of

Salmonella infection were reported after mid-July.

There is no definitive proof as the source of the

Salmonella infections but it was accepted that the deficien-

cies in the kitchen hygiene were a major factor in the

outbreak. Whether or not the turkey rolls were the source of

infection is a matter of conjecture although in other places

frozen poultry rolls that have been insufficiently thawed or

cooked have been associated with Salmonella outbreaks. It

was unfortunate that the local public health authority was

unable to mount an investigation. The tour operator has no

power to close a hotel although they can withdraw their

clients. The owners of the hotel were very cooperative and

had not appreciated the level of poor hygiene in the kitchen.

The incidence of STD in hotel guests rose above the resort

average in June and July. The hotel affected was hotel 3 in

Table 4.

6.4 1990–2000 Dominican Republic

The major tour operators introduced the Dominican

Republic as a destination in the late 1980s. In 1990, the

incidence of STD was 40% for summer season, rising to

46% in August. This is compared with a seasonal level of

2% for Florida, another new destination.

In the Dominican Republic there was very little difference

between resorts or individual hotels suggesting possible

inadequacies in the public health infrastructure, especially

the water and sewage systems. A visit was made by a tour

operator consultant in 1991 to gain an understanding of the

general public health infrastructure and hotel hygiene

standards. Discussions were held with the Secretary of

State for Tourism, senior officials within the Ministry of

Health, the Pan American Health Organisation representa-

tive, the Hotel Owners Organisation, the national water

authority and the tour operators. Major inadequacies were

identified, not least of which was the intermittent electricity

supply with no reliable back-up system. This affected

pumps for water and sewage as well as the functioning of

cold storage facilities.

Some of the hotel kitchens had very poor standards, with

no understanding of food hygiene principles by the staff. It

was concluded that there was a very real possibility of both

food and waterborne infections occurring. The housing and

facilities for hotel staff were such that levels of personal

hygiene accepted as normal in Europe could not be achieved.

There was some official acceptance by government repre-

sentatives of the situation and an indication that action

would be taken.

Over the next few years, little improvement was observed

in spite of numerous consultant visits and discussion with a

succession of Ministers of Health and of Tourism. Tour

operators identified those hotels that posed the greatest risk

and removed them from their programme. The destination

remained popular with tourists, but the incidence of STD

was unacceptably high and evenly spread amongst the

hotels. The reason for this high incidence was not identified

and there were no facilities or resources for a thorough

investigation. Various hypotheses were, however, consid-

ered. These included inadequacies in the public health

infrastructure. In particular, the water and sewage systems

and the level of kitchen hygiene and food hygiene practices

in the hotels were deficient. In some of the tourist areas a

new public water supply was constructed supplying both the

20S R.Y. CARTWRIGHT


hotels and the indigenous population, but there was no

measurable impact on the STD levels. The water supplies in

other areas were variable with many hotels relying on their

own shallow wells. Chlorination within hotels and ultraviolet

light treatment was frequently used, but was uncontrolled.

On-site testing, with a portable laboratory, usually indicated

the presence of coliforms, and occasionally E. coli, in hotel

water systems. Tour operators recommended that guests

should only use bottled water. Ice remained a problem, as

many hotels had their own ice making machines using their

own uncontrolled water. The water supplies to some of the

villages where the hotel staff lived was intermittent or by

water lorry. The quality of the supply was unknown, but on

general grounds regarded with suspicion. A few sewage

disposal systems serving groups of hotels were in existence

although many hotels had their own treatment plants.

The public health departments had insufficient resources

or trained inspectors to visit hotels and advise on food

hygiene. Inspections by hygiene consultants employed by

tour operators revealed that in most hotels there were major

deficiencies in the kitchen facilities and the food hygiene

practices in most, but not all, hotels.

In 1998, members of the Federation of Tour Operators

decided that, if they were to continue to offer holidays to

this destination, a comprehensive food hygiene-training

programme was necessary. They all adopted a common

policy that they would only use hotels that contracted with

Cristal International, a commercial food hygiene training

and auditing company. Hotels that did not agree were

removed from all the operators’ programmes. Initial

inspections by Cristal International revealed that many

hotels would require major refurbishment of kitchen areas to

enable basic food hygiene practices to be achieved and to

progress to a HACCP (Hazard Analysis Critical Control

Point) approach (WHO 1997). In the first 4 months of the

programme 13 500 food handlers were given basic food

hygiene training, the majority receiving such training for the

first time. It was discovered that the training needed to be

repeated regularly because of a large staff turnover. Training

was also provided for government health inspectors. This

initiative has been maintained, although alternative consult-

ants are now acceptable. Many hoteliers who were initially

hostile to this approach, particularly as capital expenditure

was necessary to upgrade kitchens, have found that parti-

cipation in the programme has proved to be a marketing

advantage. Ministers in the Dominican Republic govern-

ment have expressed their support for the programme. As a

result of this action a reduction in the incidence of STD was

observed and the number of ‘food poisoning’ complaints

received by tour operators declined (Table 5).

The introduction of a food hygiene programme is

universally recommended but there is little evidence to

show that, at least in the short-term, such programmes affect

the level of foodborne infection. To draw conclusions from

the experience in the Dominican Republic is largely

circumstantial in the absence of either any formal epidemi-

ological studies or any microbiological studies. The differ-

ences in STD rates are, however, at the least coincidental

with improvements in food preparation hygiene and

conform to what would have been expected on theoretical

grounds.

6.5 1991 Salmonella in flight meals

In early August 1991, reports of gastroenteritis because of

S. enteritidis phage type 6 in passengers who had flown with

two charter airlines from Corfu on 2 August were received

by CDSC (CDSC 1991). There had been 10 flights from

Corfu on that day carrying a total of 1373 passengers. The

airlines were notified by the Department of Health. Reports

were also received from other countries of similar Salmonella

illness in passengers who had flown from Corfu on that day.

All the flights involved had uploaded their flight meals from

the same supplier in Corfu. The meal served comprised: a

cold starter of fish and potato salad with mayonnaise, a main

course of stewed meat, potato, sweet corn and peas followed

by a desert of a gateau. No starters or deserts were available

for examination but a main course dish that had been deep-

frozen was examined at Guildford Public Health Laborat-

ory. A Salmonella was isolated from the meal but was a

different serotype to the outbreak strain.

Questionnaires were sent from CDSC to 1200 passengers

and there was a 57% response rate. The overall attack rate

was just over 50%. The relative risks associated with foods

consumed were fish 3Æ9%, potato salad 2Æ5%, meat 6Æ7%,

vegetables 3Æ9% and gateaux 2Æ4%. The flight meal kitchen

was visited and found to be of a high standard. At this stage

the mayonnaise used in the potato salad was considered to be

the most likely source of infection and this hypothesis was

strengthened when the chef admitted that in the week of

the outbreak he had changed from a commercial mayonnaise

to mayonnaise prepared in the kitchen from shell eggs.

Table 5 Incidence of subjective travellers’ diarrhoea (STD) in British package holiday tourists visiting the Dominican Republic during the summer

season

1992 1993 1994 1995 1996 1997 1998 1999 2000

STD (%) 43 46 48 43 57 57 38 34 29



A sample of the mayonnaise had been examined in a local

laboratory after the outbreak and Salmonella was reported to

have been isolated. A visit was made to the laboratory, which

was a small private clinical laboratory, to obtain a sub-

culture of the isolate for phage typing. The isolate had not

been retained, but it was readily apparent that the report was

meaningless as the identification relied on colonial appear-

ance on a blood agar plate. It transpired that the laboratory

staff were aware that the mayonnaise was the suspect food

and they duly obliged!

The main courses had been prepared as a large batch in

the flight meal kitchen and there were a large number of

ready to serve portions in a deep freeze. Ten meals were

examined in the UK and from two the outbreak strain was

isolated. On both occasions the Salmonella was present in

the sweet corn and peas section of the dish. This section also

contained large numbers of coliforms. The vegetables had

been prepared by cooking in bulk, the water drained off then

they were rinsed with cold water to ensure rapid cooling and

refreshing. This process took place in containers that may

have previously contained raw vegetables and salads. The

water used was from the municipality supply and had

residual chlorine of 0Æ6–0Æ8 mg l)1.

The final conclusion was that the vegetables were

contaminated during the cooling and refreshing stage. The

source of contamination was not identified although it could

have been from a previously contaminated container or from

a food operative. The initial hypothesis of the mayonnaise

was not substantiated. It was interesting and disturbing to

note that the chef and the local environmental health

inspectors had little understanding of the potential dangers

of fresh eggs. The findings of the local laboratory underlined

the dangers of using non-accredited laboratories. The

investigations in this incident were possible as the illnesses

commenced after the tourists had returned to the UK. The

investigations in Corfu were arranged by the principal

airline involved but there was good support from the local

public health department. As a result of the outbreak the

flight meal kitchen ceased trading.

6.6 Emerging pathogens in package tourism

Over the past few years two pathogens have been

associated with package tourism, and each has brought

their own particular problems.

Cryptosporidium parvum has been reported from isolated

cases of returning tourists for many years but in 2000 major

outbreaks were recorded. The diagnosis was made on return

to the UK and the information reported to CDSC at

variable rates. A relatively new feature was that in one

instance a consumer group was the first to notify the tour

operator that there was a problem but were unwilling to

assist in obtaining further information. The tour operator

was in the situation of being expected by consumers to take

action to prevent further cases of an unsubstantiated disease.

When further information was forthcoming from the

affected tourists and CDSC, it was apparent that the

outbreak was associated with only one hotel in the resort.

This indicated that the drinking water supply was unlikely

to be the source of infection. The hotel swimming pool

became the suspect source and cooperation with the local

health department sought. They stated that the pool was

satisfactory and indicated no real interest in the outbreak

although there were over 150 confirmed cases. It was not

possible for the tour operators to mount an epidemiological

study for legal reasons. Examination of hotel pool water by

Thames Water laboratories in the UK revealed the presence

of low levels of oocysts. The tour operator withdrew from

the hotel, although it continued to be used by operators from

other European countries.

In the year 2000, returning tourists reported 219 cases of

confirmed cases of cryptosporidiosis, including 106 from the

above outbreak, to FTO members from seven different

countries or major holiday regions. The majority were

associated with one of the Balearic Islands (CDSC 2000).

Hotel swimming pool water treatment processes varied but

it was recognized that spread from a faecal accident in the

pool to other bathers would occur before the water was

processed. Examination of the reported cases indicated that

in some instances the index case developed symptoms

shortly after arrival in the hotel and had travelled from a part

of the UK where cases of cryptosporidiosis were occurring.

It is possible, that in some instances, Cryptosporidium may

have been taken to the hotels by tourists.

The other ‘new’ pathogen is the Norovirus that is, at the

present time, the most problematic cause of gastrointestinal

infection in package holiday tourist. Although the spread

once introduced into a hotel or ship may be through the air,

the initial source may be food, water or an infected guest or

member of staff. Investigation of the outbreak in Andorra by

the Irish epidemiology service (Feely and McKeown 2002)

and consultants commissioned by tour operators raised the

possibility that the drinking water may have been the source

of infection. The diagnosis is generally from the clinical

presentation. Once established in a hotel it generally persists

for a few weeks with a recrudescence in the number of cases

each week as new susceptible hosts or tourists arrive. It is

not clear what the indications are for closing a hotel to break

the chain of infection, or indeed whether such a move would

be supported by resort public health authorities.

There is an urgent need for further investigation into

outbreaks of Norovirus in holiday resorts, both to identify

sources of infection and to control the outbreaks. The health

and safety committee of the FTO has produced pilot

guidelines on the management of Norovirus outbreaks in

hotels that will be tested in summer 2002.

22S R.Y. CARTWRIGHT


7. DISCUSSION

Gastrointestinal infections are regarded as the commonest

travel associated illnesses. The term travellers’ diarrhoea is

used to cover the majority of these infections and has been

the subject of many reviews (Farthing 1992; Cartwright

1993; Castelli and Carosi 1995; Cartwright and Chahed

1997) but little sustained epidemiological and microbiologi-

cal study. Studies such as that by Steffen et al. (1999) have

primarily concentrated on the presentation of the illnesses,

their duration and severity, the causative agents and the

effect of various medications. There is a lack of information

on the source of the infections and the effect of public health

measures to reduce the illness of the infections.

National communicable disease surveillance programmes

do not identify the majority of water and foodborne disease

in travellers. This is mainly because the illness is usually

self-treated, or if medical assistance is sought, laboratory

tests were not undertaken or even available. The incentive to

improve the situation has a low priority in national health

service programmes as the illnesses have a minimal effect on

the health services of a country and those affected return to

their home country within a short time. Imported infections

in returning tourists may be identified, but any investigation

is regarded as the responsibility of the local health author-

ities in the holiday destination. Travel associated gastroin-

testinal infections that are primarily food and waterborne

are, therefore, largely ignored by the Ministries or Depart-

ments of Health of most countries. Ministries of Tourism

may have a concern but, as it is a health issue, may be

powerless to take action. This has resulted in the UK tourist

industry, and in particular the major tour operators,

developing a crude surveillance system and in promoting

health and safety programmes.

Academic epidemiologists ridiculed the development of

the CSQ approach to collect basic health data 20 years ago

as being too simplistic to be of any value. Its limitations

were, however, recognized from the beginning and inap-

propriate conclusions not drawn from the results. It has

proved to be adequate for the purpose for which it was

required. The results have been used to great advantage in

identifying high-risk resorts, and in separating problems

because of deficient public health infrastructure from those

of poor kitchen hygiene in hotels. It has been possible to

monitor the health effects of remedial actions.

There have been, and still are, deficiencies in the

investigation of suspected outbreaks. What is often not

obvious is the background political manoeuvring to prevent

any investigation in some destinations. The fear of publicity,

the need for capital expenditure or the risk of senior

personnel losing their job are but some of the reasons for

these obstructions. Diplomacy becomes an essential require-

ment in the encouragement of investigations. Although tour

operators have no authority to undertake investigations in

resorts, they can arrange for consultants to inspect hotels

that have been involved in an incident. If a problem involves

more than one hotel, or is thought to have a wider

community involvement, the local health authority is

contacted and in some resorts there has been an excellent

response.

The prevention of travel-associated infections is largely

concentrated on pre-travel advice. Travel clinics and advice

from government departments (Department of Health 2000)

encourages tourists to alter their behaviour with immuniza-

tion for a few selected diseases. Dietary advice such as ‘boil it,

cook it, peel it or forget it’ as advised by Kozicki et al. (1985),

has been promulgated for many years but there is little

evidence to show that it has been effective. Indeed, it is

advice that may be very difficult to follow on package

holidays with all the food provided by a hotel. The

presentation of food dishes are often like works of art but

may contain a mixture of cooked foods and salads, the safety

of the dish relying on the preparation of the salad component.

In countries with active programmes for the prevention of

foodborne infections, the emphasis is on education and the

implementation of good food hygiene programmes based on

the HACCP principles. This in turn requires the food

preparation premises to meet required standards and a

certain level of basic education of the food handlers. The

FTO has encouraged the governments of destination

countries to develop and implement food hygiene pro-

grammes, but with limited and variable success. As a result,

part of their overall proactive health and safety programme

has been the development of a food hygiene code of practice

and auditing programme for use by their members. This is

being introduced in 2002 and will become part of the

contract between tour operators and hoteliers. It will be

complimentary to any national legislation. In the Caribbean,

a joint venture by the Caribbean Alliance for Sustainable

Tourism and the Caribbean Epidemiology Centre has

developed the Quality Tourism for the Caribbean project

that includes guidelines for food safety and sanitation (QTC

2002). They are also developing local surveillance of tourists

illnesses based on a hotel reporting system.

The World Tourism Organisation is developing an

International Food Safety Standard for the Tourism Sector

with inputs from the food section of WHO, FAO, the

hospitality industry, private consultants and tour operators.

The prevention of waterborne disease primarily depends

on the provision of a safe drinking water supply. In many

tourist areas, especially those in developing areas, this

cannot be guaranteed. Private water supplies may have little

or no control and even municipal supplies may have a level

of control that does not meet either European or American

requirements. This may be in spite of the country’s own

legislation stipulating the standards for drinking water. The



ambassador of a major tourist destination informed about a

meeting at which gastrointestinal illnesses were being

discussed, that his government could pass any laws that

were required and the solution was being implemented.

The surveillance, investigation and prevention of food and

waterborne infections associated with package holiday travel

raises many questions as to who is responsible legally,

morally and practically. The information available is by no

means clear and can vary rapidly with time. The tourists

expect that their health will be safeguarded, yet continue to

book holidays to destinations with a known high incidence of

food and waterborne infections. Those who work to improve

the situation do so with tools reminiscent of those available

to John Snow in the control of a cholera outbreak associated

with the Broad Street pump. Improvements have been made

and will continue to be made but require active public

private partnership and cross discipline cooperation at both

professional and political levels. The numbers of package

holiday tourists will continue to increase, as will the number

of destinations. Appropriate surveillance methods, investi-

gation facilities and preventative programmes need to be

developed in order to keep the levels of food and waterborne

infections to a minimum.

8. REFERENCES

Cartwright, R.Y. (1993) Travellers’ diarrhoea. British Medical Bulletin

49, 348–362.

Cartwright, R.Y. and Chahed, M. (1997) Foodborne diseases in

travellers. World Health Statistics Quarterly 50, 102–110.

Castelli, F. and Carosi, G. (1995) Epidemiology of traveler’s diarrhea.

Chemotherapy 41(Suppl 1), 20–32.

CDSC (1991) Communicable Disease Report 1, 149.

CDSC (2000) Communicable Disease Report 10, 285.

Consumers Association (1999) Sick leave Holiday Which, Autumn

1999, 184–197.

Department of Health (2000) Health advice for travellers. T6, London.

Farthing, M.J. (1992) Travellers’ diarrhoea. British Journal of Hospital

Medicine 48, 82–92.

Feely, E. and McKeown, P. (2002) Gastroenteritis in holidaymakers

returning from Andorra, January–February 2002. EuroSurveillance

Weekly 10, 1–2.

Food Standards Agency (2000) A Report of the Study of Infectious

Intestinal Disease in England, London.

Kozicki, M., Steffen, R. and Schar, M. (1985) ‘Boil it, cook it, peel it or

forget it’: does this rule prevent travellers’ diarrhoea? International

Journal of Epidemiology 14, 169–172.

McEvoy, M., Blake, W., Brown, D., Green, J. and Cartwright, R.

(1996) An outbreak of viral gastroenteritis on a cruise ship.

Communicable Disease Report CDR Review 6, R188–192.

Quality Tourism for the Caribbean (2002) Food safety and sanitation,

Port of Spain Trinidad.

Reid, D., Dewar, R., Fallon, R.J., Cossar, J.H. and Grist, N.R. (1980)

Infection and travel: the experience of package tourists and other

travellers. Journal of Infection 2, 365–370.

Steffen, R., Van der Linde, F., Gyr, K. and Schar, M. (1983)

Epidemiology of diarrhea in travelers. Journal of the American

Medical Association 249, 1176–1180.

Steffen, R., Collard, F., Tornieporth, N., Campbell-Forrester, S.,

Ashley, D., Thompson, S., Mathewson, J.J., Maes, E., Stephenson,

B., DuPont, H.L. and von Sonnenburg, F. (1999) Epidemiology,

etiology, and impact of traveler’s diarrhea in Jamaica. Journal of the

American Medical Association 281, 811–817.

World Health Organisation (1997) HACCP Introducing the Hazard

Analysis and Critical Control Point System. WHO/FSF/FOS/97.2.

World Tourism Organisation (2001) Tourism Highlights 2001, Madrid.

24S R.Y. CARTWRIGHT


Documents

Food and waterborne infections associated with package holidays