Looking for Evidence that Personal Hygiene Precautions Prevent ...

Looking for Evidence that Personal Hygiene
Precautions Prevent Traveler’s Diarrhea
David R. Shlim
Jackson Hole Travel and Tropical Medicine, Jackson, Wyoming
SUPPLEMENT ARTICLE
In the 50 years during which traveler’s diarrhea has been studied, it has always been assumed that personal
hygiene precautions can prevent or reduce the likelihood of developing traveler’s diarrhea. However, 7 of 8
studies that specifically addressed this issue showed no correlation between the types of food selected and the
risk of acquiring traveler’s diarrhea. The eighth study showed a correlation between a few dietary mistakes
and a decreased risk of acquiring traveler’s diarrhea. A further increase in the number of dietary mistakes,
however, did not continue to increase the risk of acquiring traveler’s diarrhea. Personal hygiene precautions,
when performed under the direct supervision of an expatriate operating his or her own kitchen, can prevent
traveler’s diarrhea, but poor restaurant hygiene in most developing countries continues to create an insurmountable
risk of acquiring traveler’s diarrhea.
The adage “Boil it, cook it, peel it, or forget it” has been
asserted so often as an effective method to prevent traveler’s
diarrhea that it seems almost sacrilegious to question
it. A search for this phrase on the Internet via Google
yielded 4230 references. At the time of this writing, no
one seems to be certain of the origin of the phrase, which
entered the travel medicine literature as a quotation in
a key article published in 1983 [1]. That article is often
cited as proof that how and what one chooses to eat can
influence whether one develops traveler’s diarrhea.
However, there are 7 other articles that have examined
this issue in various ways. None of them suggest
that there is a correlation between following the aforementioned
advice and a decrease in the risk of acquiring
traveler’s diarrhea. One of the articles recorded dietary
mistakes based on failure to follow pretravel advice, but
no “dose-response” relationship was established—in other
words, there was no correlation between the number
of dietary mistakes and the risk of acquiring traveler’s
diarrhea. To better understand what we know about
the prevention of traveler’s diarrhea through following
Reprints or correspondence: Dr. David R. Shlim, Jackson Hole Travel and Tropical
Medicine, PO Box 40, Kelly, WY 83011 (drshlim@wyom.net).
Clinical Infectious Diseases 2005; 41:S531–5
2005 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2005/4110S8-0003$15.00
dietary advice, it would be worthwhile to review in
detail the available literature.
METHODS
A search of the literature was performed by searching
PubMed for the key words “traveler’s diarrhea,” “hygiene,”
and “prevention.” In addition, articles that I
already had in my files were used. Eight key articles
were identified that made specific reference to studies
of the prevention of traveler’s diarrhea through personal
hygiene precautions. In this context, “personal
hygiene precautions” refers to selection or avoidance
of particular foods or drinks.
RESULTS
Eight studies addressed the issue of food precautions
and risk of acquiring traveler’s diarrhea.
Mexico, 1973. The first study, by Loewenstein et
al. [2], looked at attendees of the 10th annual International
Congress of Microbiology in Mexico City in
August 1970. The authors distributed a questionnaire
to “almost all” 2200 participants. Given the nature of
the topic, we might assume that this was a highly motivated
group. However, slightly fewer than one-half of
the participants returned a completed questionnaire. The
authors analyzed the return rate and results according
to the country of origin, and it is easier to summarize
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their results if we limit our focus to the group of participants
from the United States and Canada. Of this group, 597 (58%)
of 1029 attendees returned questionnaires. Of these 597 persons,
325 (54%) reported at least 1 episode of traveler’s diarrhea.
The questionnaire specifically asked whether the person
drank bottled liquids or avoided salads, raw vegetables, and
unpeeled fruit. The attack rate of traveler’s diarrhea among
persons who said that they took these precautions was the same
as that among those who said that they did not take these
precautions. The conclusion of these authors was that “drinking
bottled liquids, and avoiding salads, raw vegetables, and unpeeled
fruits also failed to prevent illness” [2, page 530].
Mexico, 1976. The second study, by Merson et al. [3], was
also performed at a medical conference in Mexico. The subjects
included 73 physicians and 48 of their family members who
were attending the Fifth World Congress of Gastroenterology
in Mexico City in October 1974. Traveler’s diarrhea occurred
in 59 persons (49%). This highly motivated group of participants
provided stool specimens before, during, and after their
1–2-week trip to Mexico. In addition, the 73 physicians provided
a serum sample before and after the trip.
A questionnaire was given to all participants 10 days after
they left Mexico. The questionnaire contained questions regarding
the consumption of food and water while in Mexico.
All participants completed the questionnaire. The authors concluded
that “illness was not associated with consumption of
water or iced beverages.…Illness was similarly not associated
with consumption of vendor food, salads containing raw vegetables,
other raw vegetables, or unpeeled fruits” [3, page 1303].
However, the subgroup of participants who acquired infections
with enterotoxigenic Escherichia coli had eaten salads containing
raw vegetables significantly more often than had noninfected
participants ( ). This increased risk was not associated
P p .014
with consumption of other raw vegetables or unpeeled fruits.
Mexico and Peru, 1978. Chang distributed questionnaires
to charter passengers returning from Mexico ( ) and
n p 162
Peru ( ) [4]. The questionnaires inquired about the sen
p 65
verity and number of episodes of traveler’s diarrhea and the
risk factors for acquiring traveler’s diarrhea. Eighty-two percent
of the travelers to Mexico experienced traveler’s diarrhea,
whereas 60% of the travelers to Peru reported traveler’s diarrhea.
The author noted, “Avoidance of tap water, uncooked
foods, and ice cubes did not make a difference in the outcome”
[4, page 429]. No details about individual risk factors are given.
Worldwide, 1983. Steffen et al. [5] surveyed nearly 10,000
tourists about their food precautions and risk of acquiring traveler’s
diarrhea in various destinations worldwide. For a 22month
period, a questionnaire was handed out by air crew
members on flights returning to Switzerland and Germany from
numerous international destinations. A total of 16,568 questionnaires
were distributed, and 60.2% were completed and
S532 • CID 2005:41 (Suppl 8) • Shlim
returned. The rates of traveler’s diarrhea in developing countries
were 30%–57%. Steffen et al. [5] used a unique method
of evaluating the rate of traveler’s diarrhea among tourists who
applied different levels of food precautions. The baseline rate
of diarrhea in all travelers (33.9%) was given the value of 1.0.
The results are shown in table 1. The table demonstrates that,
in a retrospective study of traveler’s diarrhea, subjects who
appeared to exercise more caution were at increased risk of
acquiring traveler’s diarrhea. Or, as the authors stated: “Thus,
diarrhea seemed to occur more frequently the more a person
tried to elude it!” [5, page 1179], Even if we ignore, for the
moment, the inverse relationship between dietary precautions
and the recall of having experienced traveler’s diarrhea, the
study certainly did not provide evidence that tourists who were
more cautious about what they chose to eat were protected
against traveler’s diarrhea.
Steffen et al. [5] also noted a differential risk between resort
hotels, even at the same general destination. A 2-month survey
of 21 hotels in Tunisia, with a minimum of 20 tourists at each
hotel during that period, revealed an incidence of traveler’s diarrhea
that varied from 26% to 89%. Thus, the source of food
(i.e., the individual hotels), not the choice of foods, appeared to
make a large difference in the risk of acquiring traveler’s diarrhea.
Worldwide (children), 1991. Data on the risk of acquiring
traveler’s diarrhea in traveling children are scarce. Pitzinger et
al. [6] performed the one study that focused on the risk and
severity of traveler’s diarrhea in a retrospective study of traveling
Swiss families. Families that had sought pretravel advice
and that had children between the ages of 0 and 20 years were
sent questionnaires within 2 weeks of their return from a trip
to the tropics or subtropics. Questionnaires were sent to households
of 446 young travelers, and 363 (81.4%) of the questionnaires
were returned and evaluated. The population of children
was stratified according to age, as follows: 0–2 years (n
p 20); 3–6 years ( n p 47); 7–14 years ( n p 46);
and 15–20
years ( n p 250).
Surprisingly, 60.1% of the respondents (n p
218) stated that they took no personal hygiene precautions.
Thirty-eight percent of the travelers stated that they regularly
employed preventive measures with regard to eating. Parents
Table 1. Food precautions taken by travelers versus the risk
of acquiring traveler’s diarrhea, compared with the average risk
of acquiring traveler’s diarrhea.
Food precaution
No. of
travelers
Risk
value P
No precautions 3382 0.88 !.001
Avoided tap water only 1518 0.97 NS
Followed 1 recommended precaution 2530 1.08 !.01
Any no. and type of precaution 5966 1.09 !.001
Took 3 precautions 1041 1.13 !.001
NOTE. The risk of acquiring traveler’s diarrhea appears to increase with
increasing adherence to food precautions. Adapted from Steffen et al. [5]. NS,
not significant.
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tended to be more cautious with their children who were !3
years old: the parents of 12 (60%) of the 20 children in this
age group said that they had consistently followed dietary
guidelines. This percentage decreased to 34%–48% for parents
of children in the other age groups.
The incidence of traveler’s diarrhea in the 0–2-year age group
was 60%, despite the added care that their parents exercised.
The rate of traveler’s diarrhea in this age group, expressed as
the risk of acquiring traveler’s diarrhea per 14 days, was 40%.
The rate of traveler’s diarrhea per 14 days in the other age
groups was as follows: 3–6 years, 8.5%; 7–14 years, 21.7%; and
15–20 years, 36.0%.
The authors looked for correlations between the families that
followed eating precautions and the rate of traveler’s diarrhea.
They concluded that “no significant differences between those
who did and did not adhere to the rules were observed in children
below the age of 15 years” [6, page 1991]. In the 15–20year
age group, the protective effect of eating precautions just
reached significance ( ).
P ! .05
Again, for reasons that are difficult to explain, young children
whose parents took the most precautions had the highest rate
of traveler’s diarrhea. This finding may be related to the increased
susceptibility to pathogens among children in the 0–
2-year age group, but, even if this is true, trying to prevent
ingestion of pathogens should decrease the rate of illness.
Morocco, 1995. When hygienic eating precautions are evaluated,
the question is always raised as to whether these rules are
capable of being applied while traveling or whether travelers are
motivated to do so. Certainly, the rate of dietary mistakes is high
where it has been evaluated. If the risk of acquiring traveler’s
diarrhea is associated with eating or avoiding certain foods or
types of foods, travelers who adhere to this advice the most closely
should be least likely to experience traveler’s diarrhea. However,
this was not the case in the study conducted by Matilla et al. [7]
among Finnish travelers to Morocco. The subjects were tourists
on package tours to Morocco for 1 or 2 weeks. Subjects were
contacted by letter prior to travel, and those willing to participate
in the study were seen by an investigator and given a questionnaire
to be filled out during the trip. The questionnaire contained
questions about the consumption of 13 different food and beverage
items. A total of 993 persons completed the study and
supplied a stool sample. However, the majority of the study
population ( ) was randomized to receive the B subunit–
n p 788
whole-cell cholera vaccine, which offers some protection against
enterotoxigenic E. coli, or placebo. Of the group who received
only placebo or no vaccine ( ), 155 (28%) developed
n p 547
traveler’s diarrhea during their trip.
The authors observed that only 46 (5%) of the total number
of travelers claimed to have made no dietary mistakes. Of
this group, 15 (33%) developed traveler’s diarrhea. The authors
stated: “the incidence of traveler’s diarrhea was not associated
with the presence or absence of any specific dietary errors or
the number of them committed” [7, page 81].
Nepal, 1996. After living in Nepal and running the main
travel medicine clinic that took care of foreigners there for 12
years, I realized that we still did not have solidly based recommendations
that could help a traveler prevent traveler’s diarrhea.
We undertook a year-long study in 1992–1993 to evaluate
risk factors for traveler’s diarrhea, focusing in particular
on the expatriate (foreign resident) population who lived at
continuous risk of acquiring traveler’s diarrhea [8]. Sixty-nine
expatriates and 120 tourists with traveler’s diarrhea were enrolled
in the study and were compared with 112 asymptomatic
tourist and expatriate control subjects. The people with diarrhea
were randomly enrolled each day if they happened to be the
first 2 patients of the day with stool soft enough to conform
to the cup used for stool collection. They were then asked to
complete a 10-page questionnaire. The control subjects were
recruited from patients at the Canadian International Water
and Energy Consultants Clinic (Kathmandu, Nepal) who presented
with a nongastrointestinal complaint, had not experienced
diarrhea for at least 2 weeks, and were willing to supply
a stool sample and fill out the same questionnaire.
The results of our case-control study of risk factors are summarized
in table 2. The traditionally mentioned risk factors—
ingestion of tap water, ice, unpeeled fresh fruit, or raw vegetables—were
not associated with an increased risk of acquiring
traveler’s diarrhea. However, the case-control method did detect
a risk from simply eating in a restaurant and from eating
other foods not previously thought to be associated with an
increased risk of acquiring traveler’s diarrhea. Eating foods that
are cooked earlier in the day and then are allowed to sit at
room temperature for a prolonged period before serving (e.g.,
quiche, lasagna, or casseroles) was highly associated with traveler’s
diarrhea. In addition, drinking a blended fruit and yogurt
drink, called a “lassi” in Nepal, was also highly associated with
traveler’s diarrhea. These positive associations confirmed the
value of the case-control method in determining risk factors.
We concluded: “Our study failed to confirm as risk factors
among residents certain foods widely believed to be associated
with traveler’s diarrhea, such as leafy vegetables, unpeeled fruits,
untreated water, and ice” [8, page 536–7].
Worldwide, 1985. Kozicki et al. [1] attempted to try to
overcome some of the limitations of memory recall associated
with questionnaires that are given to travelers after they return
from a trip and have (or have not) already experienced traveler’s
diarrhea. They distributed 2240 questionnaires to Swiss travelers
departing to a wide variety of destinations. The travelers
were asked to record their eating choices for the first 3 days
of their holiday and to note whether they experienced traveler’s
diarrhea during the first 5 days of their trip. They were then
to return the questionnaire at the end of the trip.
Six hundred eighty-eight (30.7%) of the 2240 travelers who
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Table 2. Risk factors for traveler’s diarrhea among foreign residents of Nepal.
Risk factor
S534 • CID 2005:41 (Suppl 8) • Shlim
Case patients
(n p 69)
Control subjects
(n p 87) P
Drank untreated water 6 (9) 8 (9) NS
Took ice in drink 6/67 a (9) 10 (11) NS
Ate raw vegetables 26/68 a (38) 29 (33) NS
Ate unpeeled fresh fruit 27 (39) 32 (37) NS
Ate fruit salad in restaurant 23/68 a (34) 28 (32) NS
Ate at least 1 meal in restaurant during preceding week 66 (96) 72 (83) .01
Meals eaten in restaurant during preceding week, median no. (IQR) 4 (2–7) 2 (1–5) .03
Ate foods that require reheating b
15 (22) 6 (7) .007
Drank lassi c
22/68 a (32) 8/86 a (9) !.001
NOTE. Data are no. (%) of patients or subjects, except where noted. Adapted from Hoge and Shlim [8]. IQR, interquartile
range; NS, not significant.
a Denominator used in the calculation of the percentage excludes persons who did not answer the question regarding this risk
factor.
b For example, quiche, lasagna, or casseroles.
c A blended fruit/yogurt drink.
accepted questionnaires actually returned a completed questionnaire.
As the authors concede, this subgroup of travelers
may not be representative of the entire group. We do not know
what happened to the other 1552 people. The self-selection of
travelers who decided to record their eating choices may not
be representative of the group as a whole. However, the study
is the only prospective study of eating choices in relation to
traveler’s diarrhea that has been attempted, so the authors decided
to report the results anyway.
Only 13 travelers (2%) were able to adhere to the dietary
precautions they had been given. In the group that made 0–1
dietary mistakes ( ), there were 3 cases of traveler’s din
p 51
arrhea. The rate of traveler’s diarrhea increased to 24% in the
group that made 6–7 mistakes, and it then leveled off, despite
an increase in total mistakes (for a total of 13). In other words,
a further number of dietary mistakes did not continue to increase
the risk of acquiring traveler’s diarrhea beyond the risk
that existed in association with 7 mistakes, the point at which
24% of tourists got traveler’s diarrhea.
In addition to the number of dietary mistakes made, the
study looked at particular risk factors. Drinking bottled water
was a significant risk for traveler’s diarrhea, although drinking
tap water was not. Use of ice cubes appeared to be a significant
risk. Drinking fruit juice, whether bottled or not, was not associated
with traveler’s diarrhea, neither was eating peeled or
unpeeled tomatoes. Eating peeled or unpeeled fruits was not
associated with traveler’s diarrhea. However, eating raw salads
was associated with traveler’s diarrhea in this study. In addition,
consumption of cold meats or raw meat (steak tartare) was
associated with traveler’s diarrhea, as was consumption of raw
oysters. If you look at the list of significant and nonsignificant
risk factors, there is no clear pattern that supports the adage
“Boil it, cook it, peel it, or forget it.”
DISCUSSION
Seven studies of risk factors for traveler’s diarrhea, conducted
during a 23-year period, failed to find any correlation between
following the usual dietary precautions and a diminished risk
of acquiring traveler’s diarrhea. The eighth study appeared to
show a correlation between cumulative dietary mistakes and
an increased risk of acquiring traveler’s diarrhea over a 3-day
period, but a review of the individual foods associated with
traveler’s diarrhea—for example, showing that drinking bottled
water was associated with traveler’s diarrhea whereas drinking
tap water was not—makes it difficult to understand the risks
associated with consumption of individual foods.
In an editorial accompanying the publication of the article by
Steffen et al. in 1983 [5], DuPont et al. concluded: “While food
is the major vehicle of transmission, Steffen et al. provide data
that indicate we cannot avoid the problem [of traveler’s diarrhea]
by exercising care in where and what we eat” [9, page 1194]. In
a review of the papers available to him in 1986, Blaser wrote:
“Surprisingly, the drinking of bottled liquids and the avoidance
of salads, raw vegetables, and unpeeled fruit failed to prevent
diarrhea…These results may suggest that the etiologic agents
which cause travelers’ diarrhea are so ubiquitous in high-risk
areas that preventive measures are without value” [10, page S144].
Despite the evidence and the opinions of experts, the belief
that food precautions could reduce the likelihood of traveler’s
diarrhea continued to be asserted. A consensus panel on traveler’s
diarrhea convened by the National Institutes of Health
in 1985 concluded that “data indicate that meticulous attention
to food and beverage preparation can decrease the likelihood
of developing traveler’s diarrhea” [11, page 2702]. At that point
in time, the only “data” that they could be referring to is the
article by Kozicki et al. [1]. They appear to ignore the 3 earlier
articles that failed to find such a correlation. However, the
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consensus statement went on to say, “Most travelers encounter
great difficulty in observing the requisite dietary restrictions”
[11, page 2702]. In other words, the advice must be correct,
but travelers simply cannot follow it.
Where does this leave the traveler and the travel health professional?
It appears that the risk of acquiring traveler’s diarrhea
cannot be diminished significantly by teaching travelers simple
rules to follow with regard to food choices. Either the rules are
not sufficient, or the ability to follow them is beyond 95%–98%
of all travelers. The fact that 30% of travelers who made no
dietary mistakes got traveler’s diarrhea suggests that the current
rules are insufficient, whether they can be followed or not.
On the other hand, there is no question that foods available
in developing countries are contaminated [12–14]. Moreover,
it is true that contaminated food can be made safe to eat by
cooking it, washing it, or peeling it. The observation that expatriate
residents safely eat locally obtained foods in their own
kitchens but become sick when they eat the same foods prepared
in restaurants supports the view that proper food handling
is effective. A number of studies have pinpointed the risk
of acquiring traveler’s diarrhea as being associated with dining
in restaurants in general, independent of the types of food ordered
[8, 15, 16]. Why would this be so?
The preparation and handling of food that is served to the
public present numerous opportunities for contamination that
would thwart the benefits of “boil it, cook it, peel it, or forget
it.” An examination of restaurants in Kathmandu, Nepal, reported
recently in another review [17], revealed that there were
no sinks in which employees could wash their hands after going
to the toilet. Cutting boards were not washed between cutting
up raw meat and peeling and cutting vegetables. Foods were
cooked, but then were left to sit at ambient temperatures for
extended periods because of a paucity of refrigerator space.
Windows were not screened to prevent entry of flies. Electricity
supplies were often intermittent, and power outages occurred
for hours without warning, further diminishing the protection
offered by refrigeration. Dishes were inadequately washed and
sanitized because of the absence of abundant hot water or
commercial dishwashers. Defrosting meat would sit on a refrigerator
shelf dripping juices into already cooked foods.
The sum total of these errors leads to abundant opportunities
for the spread of enteric pathogens, whether from employees’
hands, flies, or contaminated meat and produce, with ample
time available for bacterial growth to reach infective levels. One
could postulate that “boil it, cook it, peel it, or forget it” would
be good advice to someone who was purchasing and preparing
their own food in a sanitized kitchen but that it is inadequate
for travelers faced with the multiplicity of hygienic errors found
in the kitchens of many destination countries.
The finding in Kathmandu that consumption of lasagnas or
lassis was highly associated with traveler’s diarrhea suggests that
the risk factors may extend beyond conventional advice and
can only be discovered by further studies casting a wider net
of questions. Having worked in Nepal for 12 years at the time
of our study [8], I had no suspicion that drinking lassis was a
risk factor for traveler’s diarrhea until we did the study.
The earliest studies on traveler’s diarrhea were done 50 years
ago and showed an incidence of 30%–50% among travelers.
Since that time, we have learned the etiology of most cases of
traveler’s diarrhea and have developed travel medicine into a
specialty practiced by at least 3000 people worldwide, making
travel medicine information more widely available. Despite this
knowledge, the rate of traveler’s diarrhea in travelers is still
30%–50%. Clearly, a new approach to the prevention of traveler’s
diarrhea is needed if we are going to be able to decrease
the risk to travelers over the next 50 years.
Acknowledgments
Financial support. Salix Pharmaceuticals.
Potential conflicts of interest. D.R.S.: no conflict.
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