You are on page 1of 16

Journal of Infection (I99O), 21, 27-42,

A cumulative

review of studies on travellers, their experience


of illness and the implications of these findings

J. H. Cossar,* D. Reid,* R. J. F a l l o n , t E. J. Bell,~ M. H. Riding,~


E. A. C. Follett, !1B. C. D o w , ~ S. Mitchell** a n d N. R. G r i s t t t

*Communicable Diseases (Scotland) Unit, t Department of Laboratory


Medicine, "~Regional Virus Laboratory, ~ Scottish Serum Bank, IIHepatitis
Reference (Scotland) Laboratory, Ruchill Hospital, Glasgow G2o 9NB,
~lGlasgow and West of Scotland Blood Transfusion Service, Law Hospital,
Carluke, Lanarkshire ML8 5ES, **Scottish Health Education Group,
Woodburn House, Canaan Lane, Edinburgh EHIo 4SG and aftUniversity of
Glasgow Department of Infectious Diseases, Glasgow G I 2 8QQ
Scotland, U.K.
Accepted for publication 19 February I99O
Summary
A cumulative review of illness experienced by 13 816 travellers returning to Scotland
since I977, shows an overall attack rate of 36 %. Alimentary complaints predominated;
I8 % of travellers had these alone and a further IO % had other symptoms as well as
their gastro-intestinal disorder.
Higher attack rates were noted in those taking package holidays. Inexperience of
travel, smoking, more southerly travel and younger age (particularly those between
2o- and 29-years-old) were other contributing factors. A similar pattern emerged from
a I year study of hospital in-patients with travel related admissions.
Serological studies of 47o travellers showed that 20 % had incomplete immunity to
poliomyelitis; 25 % of those tested (3 I2 travellers) had serological evidence of typhoid
immunisation, 1.9 % (of 76o travellers) had antibodies to Legionellapneumophila, 64 %
(51I travellers tested) had antibodies to hepatitis A, 87 % (288 tested) had adequate
levels of tetanus antitoxin but only 4o % of the 225 travellers tested had adequate levels
of diphtheria antitoxin.
Amongst a subgroup of 645 travellers the travel agent was the most frequently
consulted source of pre-travel health advice. This carries particular significance for the
dissemination of relevant advice in view of the inadequacies found from study of the
health information in travel brochures.
These findings, viewed against the perspective of the continuing growth in
international travel, means that travellers, the medical profession, the travel trade,
health educators, global health agencies and health authorities in those countries
accepting and encouraging tourists, will be required to recognise the health
implications of further tourism development if this problem of illness associated with
travel is to be brought under control.

Introduction
T h e last few decades have witnessed a remarkable growth in international
travel. T h i s has followed increased trade, political , cultural and sports
exchanges between nations, military manoeuvres, pilgrimages, labour and
o163-4453/9o/o4oo27 + I6 So2.oo/o

I99O The British Society for the Study of Infection

28

]. H. C O S S A R E T . 4 L .

refugee movements, and more frequent tourist travel--34I million in I986


alone. 1 Growth has also been promoted by a sophisticated travel trade
combined with the speed (cruising speed of Concorde I356 m.p.h.), comfort
and capacity (400+ passengers per ' j u m b o jet') of the m o d e r n passenger
aeroplane. All these population movements have the potential for transmission
of infection and this is increased by overcrowding, inadequate sanitation
facilities, and when the climatic and cultural contrasts between home and guest
countries are most extreme, such as for example between northern Europe and
tropical Africa.
As well as the familiar problem o f ' traveller's diarrhoea' the following more
serious infections have been imported into the U.K. during the last Io years:
typhoid fever 2 hepatitis, ~-5 poliomyelitis, 6-8 leptospirosis, 9 schistosomiasis, 1' n
amoebiasis,12 cholera,13.14 rabies ~5 giardiasis,l~ salmonellosis,XT. 18 shigellosis,19
dysentery,17 leishmaniasis,20.21 lassa fever, 22' 2~ trypanosomiasis,24 legionnaires'
disease, 25-~7 diphtheria, 28'29 cytomegalovirus infection, s malaria, 31 acquired
i m m u n e deficiency syndrome, 32 and sexually transmitted diseases. 33'34
Recognising that these problems are steadily increasing for the reasons
outlined above, the Communicable Diseases (Scotland) Unit ( C D S U ) in
association with the University of Glasgow D e p a r t m e n t of Infectious Diseases,
the D e p a r t m e n t of Laboratory Medicine, the Regional Virus Laboratory and
the Scottish Health Education Group (SHEG), have, since I977, been actively
involved in monitoring the health experiences of returning Scottish
travellers 35-45 and their i m m u n i t y to infection. 26' 40.46-4s At the same time they
have looked at the adequacy 49 and ways of improving 5-52 current pre-travel
health advice. This paper presents previously unpublished studies, an overall
cumulative review, and suggests action based on these findings.
Methods

Between 1977 and I985 travellers returning to Scotland and one group of
visitors to Scotland have been issued with a standard questionnaire to record
personal and travel details which include age, gender, occupation, country,
town and type of accommodation, dates of travel, reasons for travel, pre-travel
health status, symptomatic complaints with date of onset and duration, any
factors to which illness might be attributed, and whether the help of a doctor
or hospital was required. T h e questionnaires were returned to C D S U using a
prepaid reply envelope. Most travellers were issued with the questionnaire at
their return airport (Glasgow or Edinburgh), some by travel agents, employers,
and tourism departments, and the remainder by C D S U in response to public
d e m a n d following media publicity which had highlighted specific episodes of
travel related illness. T h e questionnaire was updated to include details on
smoking habits (I98o), to make completion and computer analysis easier
(I98I), and to enquire about pre-travel health advice (I985), but the basic
information collected remained otherwise essentially unchanged t h r o u g h o u t
the period of study. This enabled valid comparative analyses to be carried out.
Initially the data collected were analysed manually, thereafter computers
were used (initially at C D S U , and latterly Glasgow University mainframe),
and the information analysed using the Statistical Packages for the Social

Studies of travel related illness

29

Sciences (SPSSx). T h e main p r o b l e m was the self-selection bias of the sample.


H o w e v e r , if the reasonable assumption is m a d e that all the groups studied have
the same response bias and an identical m e t h o d o l o g y is used throughout,
comparison within these groups can be justified. W h e r e appropriate the Chisquared (X2) test is used in a t w o - w a y table; occasionally with tests for trend
or t h r e e - w a y tables it was necessary to use log-linear and logistic models.
M o r e than 75o of the travellers from several of the studies 26' 35' 38-41'4~
volunteered a 5 ml sample of venous b l o o d in response to our request. T h e s e
were collected at Ruchill Hospital, at travellers' homes and places of work, and
with the help of their family doctors, particularly for those distant from
Glasgow. T h e serum samples thus collected were divided into portions at
Ruchill Hospital laboratories for various antibody titres to be m e a s u r e d viz,
poliomyelitis (Regional Virus Laboratory), hepatitis A (Hepatitis Reference
Laboratory), Legionella pneumophila and Salmonella typhi ( D e p a r t m e n t of
L a b o r a t o r y Medicine). T e t a n u s antitoxin levels were m e a s u r e d at the Scottish
S e r u m Bank (Ruchill Hospital), and diphtheria antitoxin levels at the Glasgow
and W e s t of Scotland Blood T r a n s f u s i o n Service ( L a w Hospital).
Neutralising antibodies to each of the three types of poliovirus were
estimated using the modified micro-metabolic inhibition test. 53 All s e r u m
titrations for the latter were started at a dilution of I in 4 (i.e. I in 8 in final
s e r u m virus mixtures) which were incubated for 3 h at r o o m t e m p e r a t u r e
followed b y overnight incubation at 4 C. All tests were carried out in parallel
with British Standard poliovirus antisera types I, 2 and 3.
T o t a l antibody to hepatitis A virus was m e a s u r e d by a competitive
r a d i o i m m u n o a s s a y ( H A V A B , A b b o t t Laboratories, Chicago),47 samples were
tested for antibody to L. pneumophila as described b y Fallon and Abraham,54
to S. typhi using a standard agglutination technique 55 except that the
incubation t e m p e r a t u r e used was 5o C.
Sera (previously stored at - 2o C) were tested for tetanus I g G ( L a b s y s t e m s
U . K . , L t d ) according to the manufacturers r e c o m m e n d e d method. T h e
controls were three sera negative for tetanus antitoxin and seven positive sera
with k n o w n antitoxin concentrations of o'oo5-5 I U / m l . Optical densities (OD)
were o b s e r v e d at 4o5 n m on a F l o w Multiscan E L I S A reader. T o determine
the i m m u n e status of an individual a o.oI I U / m l positive control was used as
the c u t - o f f point. A n individual with a test OD > the o'oI I U / m l positive
control was considered to be i m m u n e b u t susceptible if the test ratio was less
than this value.
D i p h t h e r i a toxoid sensitised cells were p r o d u c e d in a similar manner to that
described for tetanus toxoid sensitised cells b y Barr et al. 5~ H u m a n plasma
assayed as 2 I U / m l b y the National Institute for Biological Standards and
Control was used as a reference standard and a I in 2oo dilution (o'oI I U / m l )
of this material was used in all test runs. In the passive haemagglutination slide
test, 5o #1 of test s e r u m was mixed with an equal volume of 2 ~o diphtheria
toxoid sensitised cell suspension on a glass slide. After 5 min at r o o m
temperature, tests were read b y comparing with the o-oI I U / m l control.
H a e m a g g l u t i n a t i o n stronger than this control indicated the presence of
diphtheria antitoxin at an i m m u n e level (i.e. > o.oi I U / m l ) .
D u r i n g the period I January to 3I D e c e m b e r I985 the in-patient details

J.H. COSSAR ET AL.


(a)
We

Respiratory and other I%


Respiratory I%
Alimentary and respiratory 2 %

rotary 18%
Alimentary and other 8%
(N=I3 816)
Gostro-enteritis 5 8 %

(b)

Malaria 389

ther 14%

. . . . ~,...... x infection 10%


(/V=71)

Fig. I. Types of travel illness. (a), Illness reported by travellers (from questionnaire studies
from z977-z985). (b), Diagnoses recorded in in-patients (from Ruchill Hospital ID Wards
I January I985 to 3~ December I985),

recorded on the Infectious Diseases (ID) Unit Record Sheet for admissions to
Ruchill Hospital were used to compile a profile on those with a travel
associated illness. These details included age, gender, ethnic origin, diagnosis,
length of stay in hospital, whether the illness was considered to be associated
with travel, the country visited and the number of days since returning to the
U.K.
The information collected by these methods was used to define a perspective
of travellers from the west of Scotland and of travel related illnesses. Due to
the retrospective nature of the data collections, questionnaire revision and
incomplete responses, the numbers analysed under different categories o f
study, of necessity, have differing totals.
Results
Thirteen thousand, eight hundred and sixteen completed questionnaires were
returned. The response rate ranged from 2o-77 ~o amongst individual groups

Studies of travel related illness


3500~

(a)

3000~-

(b)

r,o 2500 ~T

2000~

!iiiiiiii

!i!!!i!!i

i!iii!iii

;;~;

isoo[

,ooo[ i

::::::1::

iiiii!ii!
iiiiiiii!

iiiiiii!i

i!i!iii!i!iiiiiii
i@

iiiil
E

g;
,e

..~

Age groups

Age groups

Fig. 2. Distribution of travellers by age group and illness. (a) Age of travellers and health
experience (from questionnaire studies). (IN), Total; ([]), number unwell. (b) Travel
associated admissions (from Ruchill Hospital).

with a mean of 32 %. Thirty-six per cent reported illness (low I9 % in visitors


to Scotland in i98o, 37 high 78 % - L. pneumophila study in z97726). As shown
in Fig. I, alimentary symptoms alone (diarrhoea or vomiting or both) were
reported most frequently by travellers ( I 8 % ) , a further IO% had other
illnesses associated with alimentary symptoms. Gastro-intestinal illnesses and
malaria (both 38 %) were the two most common diagnoses recorded in the inpatients studied during I985 (total with travel related illness - 7 I, i.e. 6 % of
all ID admissions).
Figure 2 shows the distribution of travellers by age group and illness, and
the age distribution of in-patients with travel related illness. In the former, the
fewest travellers were in the 0-9 and over 60 year age groups (4 and 9 %
respectively), the most in the 20-29 year group (22 ~/o) and the other groups
were closely ranged between z4 and I7 % (5 % did not give their age). T h e
20-29 year age group had the highest attack rate (48 %), thereafter attack rates
showed a progressive diminution with increasing age; those aged over 60 years
being least affected by illness (20 %). Illness was reported by 42 % of those
aged under 40 years (738I : 52 % of total travellers) and by 28 % above that age
(5764:42 %). Amongst the 71 travel associated admissions, the most numerous
were in the age group 20-29 years (25 %) closely followed by the 0-9 age group
(23 %). Altogether those aged less than 4o years accounted for 7I % of all these
admissions.
T h e gender of the travellers was documented in IO 9IO (79 %) of those who
returned questionnaires. T h e r e was no significant difference in the reports of
illness amongst the 6064 females (56 % of total) and the 4864 males (44 % of
total) - 32 and 31% being unwell respectively.

32

J. H. C O S S A R

E T AL.

Table I Illness experienced by travellers according to place visited


Summer
Unwell (%)
Scotland
Austria
Hungary
Romania
Yugoslavia
Bulgaria
U.S.S.R.
Italy
Greece
Spain
Portugal
Malta
Cyprus
Tunisia + Morocco
Other
Totals
Ranges

(I9)
-(67)
(74)
(27)
(36)
(37)
(21)
(32)
(36)
(44)
(32)
(20)
(77)
(46)
4962 (37)
(19-77)

Winter
Total

Unwell (%)

355

--

--

(20)

I3I
380
843
226
I68
637
I 194
7035
7oi
581
I20
189
914
13 4 7 4

----(I2)
--(18)
-(2i)
-(32)
-67 (20)
(12-32)

Total
-44
----50
--147
-57
-44
-342

Overall (%)
(3)
( < x)
(I)
(3)
(6)
(2)
(2)
(5)
(9)
(52)
(5)
(5)
(I)
(2)

(7)
13 816 (IOO)
( < 1-52)

T h e smoking habits of travellers were determined for IO 078 (73 %) of the


total number. Two thousand seven hundred and eighty-four (28%) were
smokers of whom 37% reported illness; non-smokers accounted for the
remaining 7294 travellers (72 %) with an overall attack rate of 32 %. T h e
higher percentage of smokers who were unwell compared with non-smokers is
statistically significant (P < o.oooI).
Reports of illness according to season of travel and country visited are
displayed in Table I. T h e most visited countries were Spain (7182 travellers:
52%) followed by Greece (II94: 9%) and Yugoslavia (843: 6 % ) ; other
countries shared between less than I and 6 % of the total. There is a trend
towards more attacks with travel further south and to some extent further east,
and this remains generally true both in summer and winter. Examples in
support of this trend are the 77 % summer attack rate reported by tourists to
Tunisia and Morocco, the 74 % for Romania, and the rate of 32 % reported
by winter tourists to Tunisia and Morocco. Attack rates in general are
substantially lower in winter (mean 20 %) than in summer (mean 37 %).
T h e relationship between the country visited and the percentage of travellers
unwell is statistically significant ( P < o-oooI). In countries having both
summer and winter travellers, the higher percentage of summer travellers who
were unwell is statistically significant for all locations except Malta (P <

0"001).
T h e majority of travellers stayed in hotel accommodation (69 % of 8870
study total), spent between I I and 15 days abroad (92 % of 9236 study total),
solely went for holiday purposes (96 % of 96o6 study total), during the
summer (96 % of I3 327 total), could be assigned to socio-economic groups i

Studies of travel related illness

33

4oo I
550
500
250
,

E 200
Z

[50
LX.X+X.:.X.>v.v.v.'.v.v.,

5O
0

.......................................
~::::1:;::::[
:.:.:.:.:.:.:31 oyo x.;:>x"
:!:!:::!:i:

l :x,x,x
~:~:~:~42..o
:~: o/c :x.:.x.:
~:~:~:~1:~:

............
:i:!:!:!:i:
3 6% ii!~!i!~!!

Travel agent
(22%)

Familydoctor
(I l%)

Other
(14%)

l.

36%

:::::::::::::::::::::::::::::::::::::::::::
!i:;:;::iii2 6 % !:;i~i....
::i::i::

Multi-source No advice token


(4%)
(56%)

Fig. 3. Pro-travel health advice, source and health experience. (Ul), Total 645; ([])~ 3I %
unwell (I99).

to 3 (66 % of 6624 total), and set off in good health (97 % of 9744 total). In view
of these findings comparisons with the minorities outside these broad
categories, which involve widely disparate proportions of travellers, require to
be interpreted with caution. T h e proportion (z 1%) who stayed in self-catering
accommodation reported a lower attack rate (26%) than those using other
types of accommodation, as did the 4 % staying abroad for more than 30 days
(23 % unwell) when compared to groups with a different length of stay abroad;
similar group comparisons revealed the lowest rates amongst those travelling
for business and holiday purposes ( < z %), IO % unwell, and in the employers
and managers, socio-economic group (9 %), 26 % unwell, compared with other
socio-economic groups. T h o s e with a pre-existing health problem (3%)
reported a higher illness rate (46 %).
Amongst the 645 travellers providing information on the use of pre-travel
health advice (Fig. 3), 284 (32 %) sought such advice of w h o m IO5 (37 %)
reported illness compared to 94 (26%) of those who did not seek advice
(56 %). T h e travel agent was most frequently consulted for advice and these
z33 travellers (22%) reported the least illness; the family doctor was least
consulted and amongst these 66 travellers (z 1%) the highest attack rate was
recorded (42 %). D u e to overlap in the numbers of travellers seeking advice
from two or more sources, the proportions in Fig. 3 add up to more than
IO0 %.

Details of the medical management of travellers were collected from 3o49


(6I %) of those who were unwell. Almost a quarter (24%) were confined to
bed, I4 % required the services of a doctor (9 % abroad, 5 % after returning),
and 61 (2 %) were admitted to hospital - - almost equally divided between h o m e
and abroad.
A total of I265 admissions to the infectious diseases wards were recorded
during the I year study period and 7I (6%), as shown in Fig. 4, were
associated with travel abroad (44 males: 62 % ; 27 females: 38 %). Amongst
both males and females the most represented group were Asians (57 and 52 %
2

JIN 21

34

J.H. C O S S A R

ET AL.

Asian)

(male Caucasian)
17;24%
3;4%
(female African)

(male African) 2

4%
ale Caucasian)
(female Asian) 14; 20%

Fig. 4. Travel associated admissions (from Ruchill Hospital). (m), Male Asian; ([~) male
Caucasian; ([]), male African; ([])~ female Asian [], female Caucasian; ([]), female African.

respectively) next were Caucasians, accounting for 38 % of the total o f these


admissions. Africans were least n u m e r o u s , (7 % of the total).
Sixty per cent o f those admitted had visited the Indian subcontinent (37 %
Pakistan: 23 % India). O f the remainder, visitors to Spain accounted for I4 %,
to Nigeria I 1 % and I6 % had visited other countries. T h e median interval
b e t w e e n return and admission was I4 days (range 1-365 days), the mean
length o f stay in hospital was 6 days (range I - 4 I days), and the total hospital
' b e d - d a y s ' accounted for b y these admissions was 432.
Between I977 and I 9 8 I , 76I travellers were tested for antibodies to L.
pneumophila o f w h o m I5 (I'9 %) were seropositive. T h e s e had r e s p o n d e d to
media publicity highlighting legionellosis and travel to Benidorm. 26
D u r i n g the period I 9 7 9 - I 9 8 2 , 47o samples were tested for poliomyelitis
neutralising antibody 4 (Table II). T h e ages ranged from I5-83 years; 55 %
were aged 3o-60 years. Eighty per cent were considered i m m u n e to infection
b u t some in each age group were susceptible to at least one serotype; two had
no antibodies. Antibodies to poliovirns types i and 3 were those most
frequently absent; 8 and I 1 % of the travellers had no detectable antibody to
these types, while 45 had no antibody to poliovirus type 2.
F r o m I 9 7 9 - I 9 8 2 , 79 (25 %) of the 3 IZ sera tested for antibodies to Salmonella
typhi were positive 4 although the levels were low except in 22 travellers with
' H ' antibodies at a titre of 160 or greater. T h r e e sera had antibody levels which
could be diagnostically confusing, two having ' O ' titres of 32o, and the other
an ' O ' titre of 4o and an ' H ' titre of 64o; no other sera had an ' O ' titre > I6O.
Five h u n d r e d and eleven samples were tested for antibodies to hepatitis A ~7
(Table I I I ) ; 64 % were a n t i - H A V positive with a range of from 3o % (age

Studies of travel related illness

35

T a b l e II Antibody status of travellers to polioviruses ~,2,3


Age group
(years)
Io-I9
20-29
30-39
40-49
50-59
6o+
Totals
Range

Without
antibody*
(%)

~ One
/ t y p e (%)

(4)
- -

- -

- -

(i)
-2 ( < I)
(o-4)

Two
types (%)

(4)
(4)
(3)
(3)
(7)
(6)
22 (5)
(3-7)

All three ~
typest (%)J

(I3)
(I8)
(I7)
(8)
(14)
(i7)

Total
number
tested

(78)
(78)
(80)
(89)
(78 )
(77)
378 (80)
(77-89)

68 (I4)
(8-18)

Overall

23
II9
66
9I
ioo
7I
470
- -

(%)
(5)
(25)
(I4)
(19)
(2i)
(I5)
(I00)

(5-25)

* At a titre of < 8.
t At a titre of > 8.

T a b l e I I I Antibody status of travellers to hepatitis A (anti-HAV)


Age group
(years)

Seropositive
(%)

Total number
tested

IO-I9
20-29
30-39
40-49
50-59
60 +
Not known
Totals
Range

(3 )
(38)
(48)
(85)
(78)
(89)
(63)
328 (64)
(3o--89)

23
I I9
66
91
I o o

71
41
511
- -

Overall
(%)
(5)
(23)
(I3)
(I 8)
(20)
(I4)
(8)
(IOO)
(5-23)

group io--I 9 years) to 89 % (age group over 60 years). T h e r e was a rise in


seropositivity with increasing age apart from a slight dip in the 50-59 year age
group. T h e prevalence of a n t i - H A V in those aged u n d e r 4o years c o m p a r e d
with those over 40 years was 4o and 83 % respectively. N o difference of note
was recorded in average seropositivity b e t w e e n earlier (I979) and later samples
(x983).
E i g h t y - s e v e n per cent of the 288 serum samples analysed for prevalence of
tetanus antitoxin had adequate levels; this encompasses a range of from 74 %
(lowest) in the 40-49 year age group, to Ioo % (highest) in the 3o-39 and 50-59
year age groups.
T w o h u n d r e d and t w e n t y five samples were tested for prevalence of
diphtheria antitoxin, 40 % of which had levels considered to be protective.
T h e s e ranged b e t w e e n 32 % in the 2 0 - z 9 year age group and 55 % in the 40-49
year age group.
2-2

36

j.H. COSSAR E T

AL.

Discussion

T h e epidemiological patterns which emerge from this comparative analysis


reported by travellers within different component study groups, with regard to
variations by type of illness, age group, country visited, season of travel,
lifestyle factors, hospitalisation, pre-travel health advice and serological
i m m u n i t y to infections, help to define the perspective of travel related illnesses
and associated risk factors. It thereby becomes possible to suggest ways in
which improvements may be made in protecting and advising the traveller.
T h e 28 % attack rate from alimentary ailments (alone or in association with
other symptoms) is the same as that reported in a study of travellers' diarrhoea
(16568 randomly selected Swiss travellers), by Steffen et al. 57 T h e rates
reported by other researchers range from I8 %58 (2665 Finnish travellers) to
4I %59 (2814 Scottish holidaymakers). T h a t this is the problem most likely to
afflict the traveller is also confirmed by Cvetanovic's estimate that in
Mediterranean countries of the European region of the World Health
Organization the yearly n u m b e r of people affected by diarrhoea is I2 million
in a population of 242 million, and that tourists coming to these areas from the
rest of Europe run a risk of developing diarrhoea 2o times greater than in their
h o m e countries. 8 This emphasises the potential for the transmission of other
gastro-intestinal infections, including typhoid and paratyphoid fevers, as well
as the spread of hepatitis A, in the increasingly popular and crowded holiday
areas of the Mediterranean coasts.
F u r t h e r confirmation of these trends in travel related illnesses is revealed by
analysis of laboratory isolates of pathogens from travellers collated at the
C D S U , which shows that between I 9 7 5 and I986 there has been a five-fold
increase in the annual total of reports (I35 and 7o4 respectively) and a
proportionate rise from 62-90 % in the reports relating to holidaymakers 61' 62
(improved reporting may also contribute to this increase). If the areas visited
by these travellers are compared, the isolates from those visiting southern
Europe now comprise 45 % of the total compared with 26 % in I 9 7 5 . T h e r e is
less proportionate change for those visiting other areas. A cumulative review
of the pathogens isolated since I975 shows that infections associated with
inadequate food handling and poor water supply or sanitation account for
87 % of these reports (total n u m b e r 492I).
T h e relaxed attitudes and reduced inhibitions which are natural elements of
vacational enjoyment expose the traveller to risks which he might otherwise
avoid, and they undoubtedly contribute to the illnesses he may acquire, with
the more adventurous, the less i m m u n e and the less experienced likely to
suffer the highest attack rates. F u r t h e r confirmation that smoking is a marker
of those with higher risk life styles (either by volition or default) is p r o v i d e d
by the smokers' significantly greater incidence of travel related illnesses as
recorded in this study.
This study and others already mentioned 57'59 which specify the most
affected age group agree that it is between 2o and 29 years of age, arguably
those likely to have the highest risk life style. This is supported by other data
analysed at the C D S U and presented at a Conference on International Travel
Medicine (Zurich, April I988), which showed that whilst the second most

Studies of travel related illness

37

frequently recorded cause of death in travellers (total study numbers 395


persons; I98o-I985) was 'accidents and injuries' (I8 ~/o), the 2o-z9 year age
group had the highest mortality from this cause. ~4
T h e r e is similar study agreement when the area is specified in that travel to
north Africa 57' 58 or eastern Europe 59 produces the highest attack rates. T h e
geographical impact of climatic contrast, and the environmental impact of
cultural contrast reflected in the higher attack rates recorded in travellers
returning from areas having the greatest contrasts to their home country,
suggest that the greater the physiological stresses and the more unfamiliar the
contact with environmental pathogens, the more illness is experienced
(however, the virulence and dose of pathogen(s) is clearly of importance). This
hypothesis is also supported by the similar attack rate trend seen in winter
travellers, and also the lower winter attack rates in general when compared
with summer travellers, both overall and for individual countries.
T h e studies showed no significant correlation between travellers reporting
illness and their gender, reason for travel, type of accommodation used, socioeconomic status or their length of stay abroad, although the highest attack
rates were recorded in those who were unskilled or unemployed, and those
who set off with pre-existing ill health. More controlled studies would be
required to corroborate any vulnerability to illness in travellers compromised
by either poor health or economic factors.
T h e pattern of illness in those admitted to hospital following return from
abroad mirrors that seen in the questionnaire studies, viz the 20--29 year age
group was the most represented and the majority presented with alimentary
symptoms. Comparatively it is of interest to note that in a review of overseas
visitors admitted to a London hospital during I986, 45% had infective
illnesses (the largest single group), many of these infections were tropical, and
the 2I-4o year age group was the most represented, 63 which is not dissimilar
to the pattern seen in this study. Although no specific denominators are
available for the Ruchill Hospital admission data, when one considers that the
majority of U.K. residents are of Caucasian extraction and do not travel
beyond Europe, 64 there is a disproportionate representation of those
contracting malaria, of travel to the Indian subcontinent, and of Asian
extraction amongst this group. This carries clear implications in terms of the
current inadequacy in giving an 'at risk' group pre-travel health advice
appropriate both in language and culture.
T h e disappointing finding that more illness was reported by those taking
pre-travel health advice than by travellers who did not suggests that there is
considerable scope for improving the quality of that advice, although perhaps
those not seeking it were more experienced and knowledgeable about avoiding
illness whilst abroad. Also of note was that the family doctor was asked for
health advice least often, and the travel agent most often. This carries obvious
implications as to the most suitable place where the traveller may obtain
advice. Surprisingly, the minority who consulted their family doctor reported
the highest attack rate, but perhaps members of this group were the least fit of
the travellers and therefore the most vulnerable to illness. Most travellers
make their arrangements via a travel agent and the health advice given by the
latter is therefore of crucial importance. Other studies have revealed

38

,1. H. C O S S A R E T A L .

inadequacies in both the quality and consistency of advice appearing in travel


brochures, 49 and, by way of example, have resulted in a general, pre-travel
health advice booklet being designed, produced and test-marketed by the
C D S U in association with the Scottish Health Education Group. 5 This
advice complements that contained in Department of Health leaflet T A I . All
the necessary specific pre-travel health advice can be provided by the informed
general practitioner who has access to free, regularly updated, information
charts, 65 or, for more complex itineraries, to the CDSU computerised database
which is updated weekly. 6~As the general practitioner is primarily responsible
for the health care of the returning traveller who is ill and has access to the
relevant past medical history and vaccination record, he is the best placed to
give appropriate medical advice to the departing traveller.
T h e economic benefits of effective advice can be measured against the
estimated IO million hospitalisation costs from travel associated admissions
based on calculations of the numbers requiring hospital care and their average
costs in I986. 45 This figure takes no account of the considerable additional
costs accruing from primary care and specialist consultations, laboratory
investigations, drug prescriptions, loss of working days and loss of vacation
time due to such illness.
Specific medical advice depends upon the travellers' pre-existing health
status, immunity to infection and exposure risk which is affected by life style.
Some diseases less common in one country are more prevalent in another,
which may lead to problems when travellers become complacent about
immunisation before travelling to countries where the disease is more
common. By way of example, 28 773 cases of paralytic poliomyelitis were
reported to the W H O in 1986, 67 whilst poliomyelitis antibody studies reported
here show that one in five of this group of travellers was incompletely immune.
Similarly three in four of those tested had no evidence of successful
immunisation to S. typhi despite the fact that at the time of testing (I982),
63% of visits carried out by U.K. residents were to countries where
immunisation was recommended. 6s In this same context one in eight of
travellers tested were at risk from infection with tetanus and two in three from
infection with diphtheria. T h e antibody studies for hepatitis A suggest that
almost one in three are at risk and support the cost effectiveness of selective
screening in the U.K. before giving immunoglobulin to older travellers at risk
from hepatitis A. 48 All the serological findings require to be interpreted with
caution as immunity will vary from area to area within the U.K. and from
country to country. T h e y do however, provide a basis for assessment of the
immunity of travellers exposed to these pathogens, which might be used not
only for the protection of the traveller, but also of the native community
following his return who may be at risk from virulent strains of these imported
infections because of low levels of herd immunity.
In summary, growth of travel and the numbers affected by travel related
illnesses, some of a serious nature, mean that this subject will increasingly
demand attention from the medical profession, the travel trade, travellers and
health authorities in countries visited by tourists.
T h e traveller is most likely to have a short self-limiting episode of gastrointestinal upset. Vulnerability to travel associated illness is increased by

Studies of travel related illness

39

inexperience of travel, in those aged between 20 and 29 years, in smokers,


d u r i n g travel in the s u m m e r , and greater climatic and cultural contrast
between the traveller's c o u n t r y of origin and his holiday destination. Provision
of appropriate general advice for the traveller, which is already available, is a
shared responsibility which is best directed, in the main, t h r o u g h travel
agencies. It can be shown to be cost effective. Specific medical advice is best
provided by the i n f o r m e d general practitioner who is responsible for the
p r i m a r y care of the returning traveller who is unwell.
C o n t i n u e d monitoring of illness in travellers and provision of information
about the problem and its prevention, using traditional channels of
c o m m u n i c a t i o n and m o d e r n technology to which medical and related
disciplines have ready access is fully justified.
Increased collaboration between medical workers, health educators and
those involved in the travel trade would be a positive and efficacious
contribution to reducing illness and discomfort in travellers, as well as the
expense that this brings to international health services.
It is clear that m a n y countries benefit economically from the development
of tourism. In r e t u r n they have to accept a responsibility towards the
prevention of illnesses associated with it.
(We thank the many individuals and organisations who assisted in the questionnaire
studies. These include Mr B. J. Forteath and Mr J. MacPherson and colleagues of
Renfrew District environmental health department, Mr C. Sibbald and staff of
Edinburgh City environmental health department, Mr H. N. Battersby and staff of
the British Airport Authority, Miss M. Sinclair and staff of the city of Glasgow Public
Relations Department, the leisure, recreation, and tourism departments of Argyll and
Bute, Cunninghame District and Strathclyde Region, the Scottish Tourist Board, the
Common Services Agency, various Glasgow companies and travel agents, the British
Broadcasting Corporation, the family doctors of the travellers studied and the
travellers themselves who volunteered information about their health and agreed to
give a blood sample to help further the research.
We also wish to record our thanks to the infectious diseases consultants at Ruchill
Hospital for permission to study the Infectious Diseases Unit Record Sheets of their
patients during I985; Mr A Millar (audio-visual technician CDSU) for assistance
with the figures and tables; Dr D. Fildes and staff (Department of Computing
Science, Glasgow University), and Mr I. Cockett (formerly of the Common Services
Agency) for the computer programming and analyses required in the studies, and Dr
C. Robertson (Department of Mathematics, Strathclyde University) for statistical
assistance.
This work was supported in part by the Chief Scientist Organisation, Edinburgh.)

References
I. World Tourism Organisation. Tourism compendium, World total. Madrid. I987.
2. Communicable Diseases (Scotland) Unit. Current Notes: Typhoid. CDS Weekly Rep
x986; 86[o5: Io.
3. Chaudhuri AKR. Tourist hepatitis in the West of Scotland. Scott MedJ I978; 23 : 213-214.
4. Follett EAC, McMichael S. Acute hepatitis A infection in West Scotland. Scott Med J
I98I; 26: I35-I37.
5. Follett EAC, McMichael S, Stewart J, Cromack S. Acute hepatitis A in West Scotland in
I98I, a change in pattern. Scott Med J I983; 28: 30-33.

4o

J. H. COSSAR ET AL.

6. Public Health Laboratory Service. Communicable Disease Surveillance Centre. Paralytic


poliomyelitis acquired abroad. CDR I985; 85/39: 1.
7- Gregory MC, Spalding J M K . Poliomyelitis in adults. Lancet 1972; i: I55.
8. Grist NR, Bell EJ. Enteroviral Etiology of the Paralytic Poliomyelitis Syndrome. Arch
Environ Health 197o; 2 I : 382-387 .
9. Public Health Laboratory Service. Leptospira Reference Unit and Communicable Disease
Surveillance Centre. Leptospirosis in man, British Isles, 1983. Br M e d J 1984; 288: I984.
IO. Centers for Disease Control, Atlanta. Acute schistosomiasis with transverse myelitis in
American students returning from Kenya. M M W R 1984; 33 (3I): 445-448.
i i. Harries AD, Fryatt R, Walker J, Chiodini PL, Bryceson A D M . Schistosomiasis in
expatriates returning to Britain from the tropics: a controlled study. Lancet I986; i: 86-88.
I2. Roemmele B. Amoebiasis in Scotland, I974-I984. CDS Weekly Rep I985; 85/I7: vii-xi.
13. Public Health Laboratory Service. Communicable Disease Surveillance Centre. Cholera.
CDR I985; 85123: I.
14. Communicable Diseases (Scotland) Unit. Current Notes. Cholera. CDS Weekly Rep I983 ;
83145 : vii.
I5. Communicable Diseases (Scotland) Unit. Current Notes. Rabies. CDS Weekly Rep I986;

86134: I6.
I6. Wilson HD. Giardiasis among a party of high school pupils following a visit to Russia.
Health Bull (Edinb) I983; 41/3 : I55-I62.
17. Sharp JCM. Infections acquired abroad. Practitioner I984; 228: 749-753.
I8. Communicable Diseases (Scotland) Unit. Current Notes. Enteric Fever. CDS Weekly Rep
I986; 86]o4: 8.
I9. Communicable Diseases (Scotland) Unit. Current Notes. Gastro-intestinal illness--the
Gambia. CDS Weekly Rep 1985; 85/49: 8.
20. Communicable Diseases (Scotland) Unit. Current Notes. Leishmaniasis. CDS Weekly
Rep 1985; 8547: 9.
2I. Jones L, Davies SN, Newland AC, Jenkins GC. A narrow escape from splenectomy. Br
Med J I985 ; 29o : 687-688.
22. Public Health Laboratory Service. Communicable Disease Surveillance Centre. Lassa
fever. CDR 1985; 85110: I.
23. Cooper CB, Grandsen WR, Webster M et al. A case of Lassa fever: experience at St
Thomas's Hospital. Br Med J I982; 285: lOO3-IOO5.
24. Duggan AJ, Hutchison MP. Sleeping sickness in Europeans : a review of lO9 cases. J Trop
Med Hyg I966; 69: I 2 4 - I 3 I .
25. Lawson JHL. Legionnaires' d i s e a s e - the Benidorm episode. Scott Med J I978; 23:
121--124 .
26. Cossar JH, Dewar RD, Fallon RJ, Grist NR, Reid D. Legionella Pneumophila in tourists.
Practitioner 1982; 226: 1543-1548.
27 . Public Health Laboratory Service. Communicable Disease Surveillance Centre. Legionnaires' disease: Morocco. CDR 1985; 85145: i.
28. Communicable Diseases (Scotland) Unit. Current Notes. Diphtheria. CDS Weekly Rep
1985; 85/5I: 9.
29. Communicable Diseases (Scotland) Unit. Current Notes. Diphtheria. CDS Weekly Rep
1986; 861o8: 12.
30. Schmitz H, Kern P, Dietrich M. High risk of cytomegalovirus mononucleosis in adult
Europeans visiting tropical areas. Lancet 1985 ; ii: 503-504.
31. Phillips-Howard PA, Bradley DJ, Blaze M, Hurn M. Malaria in Britain : 1977-86. Br Med
J 1988; 296: 245-248.
32. Communicable Diseases (Scotland) Unit. Current Notes. Acquired immune deficiency
syndrome (AIDS). CDS Weekly Rep 1986; 86/06: 8-9.
33- Public Health Laboratory Service. Communicable Disease Surveillance Centre and the
Communicable Diseases (Scotland) Unit, with Middlesex Hospital Medical School
Academic Department of Genito-urinary Medicine. Sexually transmitted diseases
surveillance, United Kingdom, 1983. CDS Weekly Rep 1985 ; 85115: xi-xvi.
34. Communicable Diseases (Scotland) Unit. Current Notes. Neisseria gonorrheae, Antibioticresistant strains. CDS Weekly Rep 1986; 861o6: 8- 9.

Studies of travel related illness

4I

35- Reid D, Dewar RD, Fallon RJ, Cossar JH, Grist NR. Infection and travel: the experience
of package tourists and other travellers. J Infect r98o; z: 365-370.
36. Reid D. Tourism and illness. Proc R Soc Edinb r982; 8zB: 23-25.
37. Dewar RD, Cossar JH, Reid D, Grist NR. Illness amongst travellers to Scotland: a pilot
study. Health Bull (Edinb) I983; 4x13: x55-z62.
38. Cossar JH, Dewar RD, Reid D, Grist NR. Travel and Health: illness associated with
winter package holidays. J R Coll Gen Pract z988; 33: 642-645.
39- Cossar JH, Dewar RD, Fallon RJ et al. Rapid response health surveillance of Scottish
tourists. Travel Traffic Med Int I984; z ' * , 23-27.
4o. Cossar JH, Reid D, Grist NR, Dewar RD, Fallon RJ, Riding MR, Bell EJ. Illness
associated with international travel : a ten year review. Travel Med Int I985 ; 3: I, I3-I8.
4 I. Grist NR, Cossar JH, Reid D, Dewar RD, Fallon RJ, Riding MH, Bell EJ. Illness
associated with a package holiday in Rumania. Scott Med J x985 ; 3o: I56-I6O.
42. Cossar JH. Travel associated illnesses. J R Soc Med I988; 8I: 25o-25i.
43. Cossar JH. Travelling and touring problems. Br J Sports Med I988; 22/3: 12o--12I.
44. Paixao MT, Cossar JH, Reid D. Mortality amongst travellers from Scotland. In: Travel
Medicine (Proceedings of the First Conference on International Travel Medicine, Zurich
i988) Berlin: Springer-Verlag, x989: 65-66.
45. Cossar JH. A review of travel-associated illness. In: Travel Medicine (Proceedings of the
First Conference on International Travel Medicine, Zurich I988) Berlin: Springer-Verlag,
z989 : 5o-54 .
46. Bell EJ, Grist NR, Cossar JH, Dewar RD, Reid D. Poliomyelitis worldwide. Br Med J
~98r; z8z: 3Io.
47. Cossar JH, Follett EAC, Riding MH, Reid D. How necessary is Immunoglobulin for
travellers going abroad ? Community Meal 1989 ; ** I x : 9-12.
48. Cossar JH, Reid D. Not atl travellers need immunoglobulin for hepatitis A. Br M e d J I987 ;
z 9 4 : I5O3.
49. Reid D, Cossar JH, Ako T I , Dewar RD. Do travel brochures give adequate advice on
avoiding illness ? Br Med J I986; z93: I472.
5o. The Scottish Health Education Group. Holiday information and checklist. (A guide to good
health on holiday for travellers) I986.
5I. Cossar JH. Inadequate pre-travel health a d v i c e - - a n answer? In: Travel Medicine
(Proceedings of the First Conference on International Travel Medicine, Zurich I988)
Berlin: Springer-Verlag, I989: 544-546.
52. Cossar JH, Walker E, Reid D, Dewar RD. Computerised advice on malaria prevention and
immunisation. Br M e d f f I988; z96: 358.
53. Kyriazopoulou VG, Bell EJ. A micrometabolic inhibition test for the estimation of
poliomyelitis neutralising antibodies. Bull W H O z972; 47: I7I-r75.
54. Fallon RJ, Abraham WH. Scottish experiences with the serological diagnosis of
Legionnaires' disease. Ann Intern Med I979; 9o: 684-686.
55. Cruickshank R, Duguid JP, Marmion BP, Swain RHA. Medical Microbiology Vol 2 I2th
ed. Edinburgh: Churchill Livingstone, I975; 417-418.
56. Barr A, Dow B, Watson WC, Hunter E. Detection and quantitation of tetanus antitoxin in
blood donations. J Clin Pathol I975; z8: 969-97I.
57. Steffen R, van der Linde F, Syr K, Schar M. Epidemiology of diarrhoea in travellers.
f f A M A i983; z49: II76--118o.
58. PeltolaH, KyronseppaH, HolsaP. T r i p s t o t h e South - - a health hazard. ScandJlnfectDis
I983; x5: 375-38I.
59. McEwan A, Jackson MH. Illness among Scots holidaymakers who had travelled abroad,
summer I983. C D S Weekly Rep I987; 87]x6: 7-9.
60. Cvjetanovic B. Diarrhoeal diseases in the Mediterranean area: report on a W H O meeting.
Copenhagen, WHO Regional Office for Europe, I988 (ICP/CDS oI9/6).
6I. Sharp JCM. Imported infections into Scotland, I975. C D S Weekly Rep I976; 76126: v-vi.
62. Campbell DM. Imported infections in Scotland, I986. C D S Weekly Rep I987; 87147:
7-8.
63. Fuller GN, Journeaux SF, Corner K, Lant AF. The risks of staying in London : a review
of overseas visitors admitted to a London hospital. J R Soc Med I988 ; 8x : 267-269.

42

J. H. COSSAR E T A L .

64 . Business Statistics Office. Business monitor annual statistics. Overseas travel and tourism.
( M Q 6) Table 8A. London: H M S O , I986; x3.
65. Cossar JH, Hamlet N, Walker E. International travel medicine, ff R Coll Gen Pract I989;
39 : 259.
66. Walker E, Cossar JH, Dewar RD, Reid D. Computerised advice on malaria prevention and
immunisations. J R Coll Gen Pract I987; 37: 223.
67. World Health Organisation. Poliomyelitis in I986, x987 and I 9 8 8 - Part L I V E R I989;
64 : 273-280.
68. Department of Health and Social Security. Immunisation against infectious disease i984;
London : H M S O .