Travel Medicine and Infectious Disease (2010) 8, 161e168

available at www.sciencedirect.com

journal homepage: www.elsevierhealth.com/journals/tmid

Malaria and travellers visiting friends and relatives

Androula Pavli a, Helena C. Maltezou b,*

a
Office for Travel Medicine, Hellenic Center for Disease Control and Prevention, Athens, Greece
b
Department for Interventions in Health-Care Facilities, Hellenic Center for Disease Control and Prevention,
3-5 Agrafon Street, Athens 15123, Greece

Received 20 October 2009; received in revised form 12 January 2010; accepted 20 January 2010
Available online 19 February 2010

KEYWORDS Summary Among all travel-acquired illnesses, malaria carries the greatest burden not only
Malaria; considering the number of imported cases but also the potential of a fatal outcome. The
Imported; increased number of imported malaria cases in developed countries in the last decades has
VFRs; been attributed to the increasing number of travel to tropical destinations in combination with
Immigrants; the enormous influx of immigrants. At present, immigrants visiting friends and relatives (VFRs)
Pre-travel advice constitute the most significant group of travellers for malaria importation in developed coun-
tries, with sub-Saharan Africa destinations carrying the highest risk. VFRs typically demon-
strate travel and behavioural patterns which render them at high risk for acquisition of this
largely preventable infection. Pre-travel services are rarely sought by VFRs, whereas miscon-
ceptions that they possess life-long immunity against malaria make them less likely to receive
or adhere to antimalarial chemoprophylaxis recommendations. There is an urgent need to
increase awareness about malaria of this group of travellers.
ª 2010 Elsevier Ltd. All rights reserved.

Introduction approximately 1 million deaths, of which 90% occur in sub-

It is less than 40 years since malaria has been eradicated
from Europe and North America as a result of ecologic
interventions, urbanization, and, since the 1940s, the wide
availability of antimalarial drugs and insecticides.1,2
However, malaria remains largely uncontrolled in many
tropical and subtropical areas, with an estimated annual
global burden of 350e500 million infections and
* Corresponding author. Tel.: þ30 210 5212 175, fax: þ30 210
5212 177.
E-mail address: helen-maltezou@ath.forthnet.gr (H.C.
Maltezou).
Saharan Africa. Currently malaria is endemic in over 100
tropical and subtropical countries.3,4
International travel is growing rapidly. It has been esti-
mated that international travel will reach approximately 1
billion by 2010 and 1.6 billion by 2020, with the largest
increase in travel to tropical and subtropical areas.5 In
developed countries, the increasing number of interna-
tional travel in association with the considerable influx of
immigrants from malaria-endemic countries had a signifi-
cant impact on imported malaria cases.6,7 Currently
malaria-endemic countries are visited by more than 125
million international travellers each year,8 whereas more
than 30,000 malaria cases occur in European and North
American travellers each year.9 Travellers visiting friends

1477-8939/$ - see front matter ª 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.tmaid.2010.01.003
162
and relatives (VFRs) account for up to 50% of international
travellers from developed countries.10e13 In the last decade
an epidemiological shift has been noted, with VFRs travel-
ling to malaria-endemic countries accounting for an
increasing proportion of cases of imported malaria in
developed countries.6,11,12,14e26 At present, VFRs are
emerging as the most significant group of travellers for
importation of malaria in non-endemic countries.7,12,26e32
The aim of this report is to review the burden and trends
of malaria associated with VFRs in developed countries.
Epidemiologic and preventive aspects are discussed.
Methods
A computerized search of the MEDLINE database through
June 2009 was conducted using combinations of the words
‘‘imported’’, ‘‘malaria’’, ‘‘international travellers’’, and
‘‘VFRs’’. Publications presenting original data on malaria in
VFRs were selected for review. Original articles were also
identified from the reference lists of articles selected
through the MEDLINE search. Review articles and book
chapters were used. Data from public health organizations
and travel statistics were also reviewed. Review of the
literature revealed that apart from VFRs, terms used
frequently include ethnic travellers, migrants, immigrants,
foreign-born travellers, and non-nationals. In the current
review VFRs are defined as immigrants living in a developed
country, distinct ethnically and racially from the majority of
population, who return to their homeland to visit friends and
relatives.33 This group is also comprised by their children,
either foreign-born or born in the country where they reside.
Immunity exists in travellers who are recent immigrants born
in malaria-endemic areas or in long-term travellers travelling
from non-endemic to endemic areas with repeated malaria
episodes. Non-immune travellers are short-term travellers or
children of migrants born in a non-endemic area.21
Epidemiology and global burden of malaria
Malaria is a parasitic disease transmitted to humans by the
bite of Anopheles mosquitoes, predominantly between
dusk and dawn. Four Plasmodium species (P. falciparum,
P. vivax, P. ovale, and P. malariae) cause malaria in
humans. Recently a fifth species, P. knowlesi, was impli-
cated in human disease in Southeast Asia.34,35 There are
also reports of imported simian malaria among travel-
lers.36,37 Infection is caused predominantly by P. falciparum
in sub-Saharan Africa and P. vivax in Southeast Asia, Central
and South America, and the Indian subcontinent.38 Infec-
tion with P. malariae or P. ovale is rare. Severe disease
concerns almost exclusively infection with P. falciparum,
although P. vivax may cause life-threatening infections
occasionally.4 In areas of stable transmission (most of sub-
Saharan Africa, and parts of northern India, Indonesia,
and South America), repeated mosquito bites provide some
immunity throughout adulthood and thus severe disease
concerns almost exclusively young children and newly
arrived persons. In contrast, in unstable endemic areas
(parts of India, Southeast Asia, Central and South America)
transmission varies greatly from year to year and severe
disease may occur throughout life.1,4
A. Pavli, H.C. Maltezou
Despite the advances noted in several control pro-
grammes at country level, the global human and economic
toll associated with malaria remains profound.2,3 In the last
decades, the emergence and spread of resistance to
common antimalarial drugs and insecticides in almost all
endemic areas in association with the lack of a vaccine for
clinical use has compromised further malaria control.1,2,4,12
Currently, malaria risk exists in 109 countries in Africa,
Asia, the Middle East, Eastern Europe, Central and South
America, the Caribbean, and Oceania.3 Sixty percent of
malaria cases worldwide occur in sub-Saharan Africa and
typically involve children under 5 years and pregnant
women, groups that carry the highest morbidity and
mortality of this disease.3,4,39 Overall, malaria causes 2% of
all deaths worldwide, with an estimated more than 2000
young lives lost daily and global direct losses of 12 billion
US$ each year.2,3,6
Malaria and VFRs
Since the 1980s, the incidence of imported malaria has
increased steadily in many developed countries. For
example, the number of imported cases reported to the
United States Centers for Disease Prevention and Control
(CDC) increased from 930 in 1982 to 1564 in 2006 cases per
year 6; similarly, 477 compared to 5898 imported cases
were notified at the National Institute of Health in Italy in
1989 and 1997, respectively.7 These numbers may be
underestimated because of underreporting or differences
in surveillance systems, and also because a number of cases
may develop while abroad. The increasing trends are
attributed to the rapid growth of international travel to
several tropical areas, reflecting on one hand the increasing
popularity of these destinations among citizens of devel-
oped countries, and on the other hand the increasing
number of immigrants from malaria-endemic countries to
developed countries. Additional reasons include changes in
travel patterns (e.g. more adventure travels and eco-
tourism) and more intense malaria transmission in certain
endemic destinations.5e7,15e17,22,24e29,40,41 Furthermore,
the increasing influx of immigrants from malaria-endemic
countries constitutes the pool for the increasing numbers
of VFRs. In the United Kingdom, a three-fold increase of
VFRs has been recorded from 1982 through 2002.41 Given
the global immigration trends towards developed countries
and the expected improvement of the immigrants’ income,
it is expected that this group of travellers will expand
further.
During the past two decades a shift in the profile of
imported malaria in developed countries has been noted,
with an increasing proportion of cases involving
VFRs.6,12,15e19 Currently, VFRs are emerging as the most
significant group of travellers for importation of malaria in
non-endemic countries.12,24,25,40 We found in the MEDLINE
14 original studies reporting data on malaria among VFRs
(Table 1); of them, 8 were from Europe, 5 from North
America, and 1 from Australia.6,7,11,16,18,20e22,24,26,27,28e
30,42
A summary of their data revealed that VFRs accoun-
ted for 21.1e68.3% out of 54,221 reported imported
malaria cases from 1984e2007, where such information was
available. Significant variations in the proportion of VFRs
among imported malaria cases were observed, even within
 Malaria and VFRs
Table 1 Original studies of imported malaria cases among VFRs.
Country Year (s) No. of % of international % of VFRs Area of infection Appropriate Severe casesc
of study cases travellersa (%) chemoprohylaxis (%)/fatality
(%)b rate(%)
Australia22 1990e1994 246 100 36.6d Asia 40 NR 2.46/0
Africa 13
America 2
Papua New Guinea 35
Solomon islands &
Vanuatu 9
Multiple countries 2e
Greece42 2005e2007 75 100 56 Africa 57 NR NR
Indian
Subcontinent 43
Italy16 1984e1993 175 100 21.1 Africa 91.4 1 9.1/0
Americas 4.0
Pacific islands 2.3
Southeast Asia 2.3
Italy7 1989e1997 5898 97.8 66.9 Africa 88.4 40 NR/0.93
Asia 8.2
Americas 2.6
Oceania 0.4
Europe 0.4
Italy21 2000e2004 380 100 40,5 Africa 94,5 26.2 23/0
Asia 4,5
Oceania & Americas 1
Spain30 1989e2005 1579 99.9 40.7 Africa 77,5 3.1 NR/0.045
Asia 7,3
America 9
Oceania 0,2
Unknown 6

Switzerland20 1994e2004 109 88.9 33 Africa 82 NR 37

Asia 5
Middle East 2
Americas 2
Unknown 10
Switzerland58 2004e2005 22 100 63.3% Africa (mainly) NR NR
The Netherlands18 2000e2002 302 100 68.3 Sub-Saharan NR NR
(4.8: children Africa 86
of VFRs) Asia 7.8
Americas 6
Unknown 0.2

163
(continued on next page)
 164
Table 1 (continued )
Country Year (s) No. of % of international % of VFRs Area of infection Appropriate Severe casesc
of study cases travellersa (%) chemoprohylaxis (%)/fatality
(%)b rate(%)
United Kingdom24 1987e2006 39,300 87.4 33.6 Africa 71.6 31 NR/0.46
(reported South Asia 24.6
travel Far East &
history) Southeast Asia 1.6
Americas &
Caribbean 1.01
Oceania 1
Middle East 0.2
United States26 2004 1324 99.6 52.6f Africa 68 19.9g NR/0.03
Asia 14.5
Americas 14.5
Oceania 3.0
United States29 2005 1528 99.8 66.9f Africa 66.9 20.9g NR/0.45
Asia & Middle
East 15.1
Americas 15.8
Oceania 2.0
United States6 2006 1564 100 50.9f Africa 69.6 20.9g NR/0.045
Asia 18.0
Americas 10.5
Oceania 1.9
United States11 2007 1505 99.9 62.8f Africa 64.4 20.3g NR/0.06
Asia 21.9
Americas 11.3
Oceania 2.3
NR: not reported.
a
Those with reported travel history.
b
According to destination and duration of travel.
c
As reported by the studies ccording to destination and duration of travel.
d
Born in a country with endemic malaria.
e
Travel in  3 other areas.
f
Out of US civilians.
g

A. Pavli, H.C. Maltezou

Out of travellers in whom this information was available.
Malaria and VFRs
the same country (e.g. 21.1e66.9% in Italy), which may be
attributed to differences in migrant populations across the
reporting countries. Most cases (57e94.5%) were con-
tracted in Africa,6,7,11,16,18,20,21,24,26,28e30,42 with the
exception of Australia, where Asia and Papua New Guinea
constituted the most frequent areas of acquisition of
infection (40% and 35% of cases, respectively).22 Overall,
Asia was the second most common area of acquisition of
infection, accounting for up to 26.2% of cases (Table 1).
Similar data have been reported by the GeoSentinel
Surveillance Network and the European Network on
Surveillance of Imported Infectious Diseases.15,25,40 As
a rule, the country of acquisition of malaria infection
among VFRs corresponds with their country of origin. Due to
the enhanced movement of populations between several
developed countries and their ex-colonies (e.g. between
Spain and Equator Guinea, and between France and the
Comoros Islands), a considerable proportion of cases are
acquired in the latter, mainly among VFRs.43,44 Malaria is
contracted predominantly in rural areas; however, trans-
mission may occur in urban areas of sub-Sahara Africa, and
to a lesser extent in urban areas of India.45
Imported malaria cases in developed countries demon-
strate seasonal patterns, that are determined by the timing
of travel as well as the season of malaria transmission in
travel destinations: imported P. falciparum cases peak in
September and January, whereas imported P. vivax cases
peak during summer.24,44 Symptoms of P. falciparum
malaria develop most often within 30 days after arrival,
whereas malaria caused by P. vivax may manifest several
months or even a year later.11,38
Studies show that P. falciparum account for the majority
of imported malaria cases acquired in Africa.24,25 Using the
GeoSentinel surveillance network database and statistics
from the World Travel Organization, the relative risks for
acquiring malaria per region visited compared with a very
low-risk area (e.g. Europe, North America) were as follows:
Sub-Saharan Africa: 208, Oceania: 77, South Asia: 54, Central
America: 38, Southeast Asia: 11.5, and South America: 8.25 A
recent study of 17,009 imported malaria cases in children
18 years in 11 developed countries (8 European countries,
Australia, United States, and Japan) during 1992e2002
showed that the highest risk for acquisition of infection were
the Comoros Islands (1030/10,000 arrivals), followed by
Democratic Republic of Congo (778), Central African
Republic (444), and other African destinations.46 Of all
paediatric cases with known country of infection, more than
75% were acquired in Africa, mainly West Africa, whereas the
majority of children were migrants VFRs.46 Children VFRs
account for a considerable number of imported malaria cases
in developed countries.11,21,23,30 In an Italian study of 337
adults and 43 children with malaria, children VFRs develop
significantly higher parasitaemia and significantly lower
platelet counts compared to recent immigrants (p Z 0.016
and 0.042, respectively); in addition, time of parasitaemia
clearance and duration of fever were longer in children VFRs
compared to recent immigrants (p Z 0.014 and 0.0085,
respectively).21 In this study, the ratio of severe to uncom-
plicated malaria cases was highest in the paediatric age
group.21 Due to lack of any exposure to the parasite in the
past, children of migrants raised in developed countries are
at high risk for severe malaria.
165
Migrants from highly endemic areas generally develop
disease-modifying immunity that diminishes malaria-
related morbidity and mortality. Such immunity is lost
progressively after a long period in the absence of repeated
exposure to infective mosquito bites; however there is
evidence that it still offers some level of protection.17,21
Long- lasting immunity has been found in VFRs who reside
in non-endemic countries for at least four years, irre-
spective of the frequency of visits to their native country.47
It has been found that VFRs are less likely to develop
complications (3.7% versus 6.3%) 15 or a fatal outcome
(1.2% versus 2.3%) compared to non-immune travellers.7
Parasitaemia was also significantly lower in VFRs
compared with other travellers in a study from Italy (mean
levels of P. falciparum parasitaemia: 996 versus 9103;
p < 0.001).17 Clinical and parasitological findings vary in
relation to the status of immunity to malaria. Immune VFRs
tend to develop significantly lower parasitaemia
(p Z 0.0032), shorter parasite clearance time (p Z 0.025),
and shorter duration of fever (p Z 0.0026) compared to
non-immune VFRs.21 Overall, VFRs with malaria develop
less often complications or have a fatal outcome compared
with non-immune travellers.15,24
Why are VFRs at higher risk for malaria?
VFRs travel frequently to rural areas with high malaria
transmission rates, away from popular tourist destinations
where living standards are far below those encountered in
their country of residence and mosquito bite precautions
may not be available. They demonstrate typical travel and
behavioural patterns, which render them at high risk for
acquisition of infection. Unless they use appropriate
protective measures and adhere to chemoprophylaxis, in
reality their risk for contracting malaria approximates the
risk of the local population. Compared with other travel-
lers, VFRs are younger, more likely to travel for longer
periods and with their children or send their children to
their family members in their country of origin. They are
also more likely to stay at local people’s homes and less
likely to travel on an organized trip.25,30,40,42,48
In addition to higher exposure, VFRs are less likely to
take adequate preventive measures.49 No use of malaria
chemoprophylaxis, or inadequate chemoprophylaxis, in
terms of appropriate drug choice or adherence to it, is
a common denominator in all studies of imported malaria,
and it was reported by 59e99% of travellers with malaria
reviewed by us (Table 1). VFRs are even less likely to use
antimalarial chemoprophylaxis compared to other travel-
lers (4% versus 36% among Italian citizens in a study).7
VFRs rarely seek pre-travel medical advice. A survey
conducted in immigrants in Italy, revealed that the length
of stay was the only factor associated with the use of pre-
travel advice and chemoprophylaxis among them.50 They
may face difficulties in accessing health-care services
because of economic, cultural, language, or legal issues.
A significant reason for not seeking pre-travel advice is
cost.25,40,42,50 Misconception about life-long immunity
against malaria is popular among immigrants.10,30,48
A survey of immigrants travelling from Canada to India,
revealed that although 69% of them considered malaria as
166
a moderate to severe illness, 41% believed that they were
not at risk for acquisition of infection.49 In this study,
intention to use antimalarial chemoprophylaxis or measures
for protection from mosquito bites were reported by only
31% and <10% of them, respectively.49 Prescription of
inappropriate chemoprophylaxis is also common.49
Assessment and prevention of the risk of malaria
There are several factors which influence the risk for
acquisition of infection, including country destination,
areas visited, season and duration of travel, type of
accommodation (e.g. camping, air-conditioned hotel), and
involvement in outdoor activities. Furthermore, accessi-
bility to health-care services is also very important with
regards to acquisition of infection.
Malaria in travellers is largely a preventable infection.
Malaria prevention for VFRs relies on: increasing awareness
about malaria risk in travel destinations, preventive
measures to reduce mosquito bite, antimalarial chemo-
prophylaxis, and prompt diagnosis and treatment.31
Mosquito bites can be prevented by using appropriate
insect repellents, bed nets, and clothes. N,N-dieth-
ylmetatoluamide (DEET) is the most effective insect
repellent, offering protection for up to 12 hours at 50%
concentration. DEET is safe for use in infants 2 months,
pregnants and breast-feeding women.31,51 Clothing that
covers most of the body surface should be worn, especially
between dusk and down. Clothes may be sprayed with
permethrin. Pregnant women and parents with young chil-
dren should be discouraged from travelling to malaria-
endemic areas if possible 46,52; if travel is inevitable,
repellents, insecticide-treated bednets (ITNs), and
chemoprophylaxis should be strongly recommended.
When accommodations are not screened adequately or
air conditioned, such as those visited by VFRs in rural areas,
it is essential to use bednets. Pre-treated, long-lasting ITNs
are most effective and can be purchased prior to travelling,
or sprayed after. Bednets should be strong and with a mesh
size of <1.5 mm and tucked under mattresses. It is partic-
ularly important to emphasize the use of ITNs for VFRs
travelling for long periods.53
Malarial chemoprophylaxis is the most effective strategy
for the prevention of severe complications and death
caused by P. falciparum malaria, and should be adminis-
tered before, during and after the exposure period (primary
chemoprophylaxis). Terminal prophylaxis is used to prevent
relapses or delayed onset malaria caused by hypnozoites of
P. vivax or P. ovale.51 Chemoprophylaxis should be selected
on the basis of individual risk, local drug resistance
patterns, and underlying medical conditions of the trav-
eller, taking into consideration the efficacy, safety, cost,
and convenience of available drugs. The development of
adverse events is a major cause of non-adherence to rec-
ommended regimens.31,51 Currently recommended drugs
include mefloquine, chloroquine, atovaquone/proguanil,
doxycycline, and primaquine.8,31,51 Mefloquine has a good
safety profile for children without age and weight restric-
tion, and a lower cost which makes it the preferred agent
for children VFRs who are more likely to travel for long
periods of time.54 It is important to stress to VFRs that
A. Pavli, H.C. Maltezou
malaria chemoprophylaxis does not prevent infection but
rather prevents clinical disease when the parasite emerges
from the liver into the blood. If medication is discontinued
sooner than recommended, a substantial risk of acquiring
clinical malaria exists.10 They should also be advised to
obtain sufficient supplies of antimalarial chemoprophy-
lactic drugs before their departure. Health-care providers
should consult the latest information on antimalarial
resistance patterns before prescribing chemoprophylaxis,
using the website of the World Health Organization or other
public health organizations.
Travellers should be informed that no preventive
measure is completely effective, and that malaria is
a medical emergency. Malaria may mimic several tropical
as well as common cosmopolitan illnesses, and should be
considered in any traveller who presents with fever or
a history of fever between 7 days after entering a malaria-
endemic area and 6 months after his return, regardless of
whether he has taken chemoprophylaxis; blood films should
be tested immediately for parasites.55 Standby malaria
treatment (or self-treatment) may be life-saving for trav-
ellers who are unable to access health-care services within
24 h after the onset of fever or those who are travelling to
areas of low-risk for malaria transmission and may be the
only affordable, tolerated option for long-term visi-
tors.8,10,51 These persons still have to access medical care
as soon as possible. Detailed instructions on the recognition
of symptoms, drug dosing and adverse effects should be
provided.8,51
Ideally, clinics attended frequently by immigrants could
offer pre-travel services, since familiarity and easy access
might encourage their use. Language barriers could be
surpassed by multi-lingual health-care providers and infor-
mation about precautions against malaria should be
disseminated through posters and leaflets. Primary health-
care providers, who may also provide travel health advice,
should take the opportunity and ask patients who were born
in endemic countries, or have ethnic links to such countries
whether they will be visiting friends and relatives in the
future and provide with relevant travel health informa-
tion.56 In urban centres which are home to large immigrant
populations, a routine screen for high-risk travel and
coordination of pre-travel care with paediatric preventive
care may help secure the best possible pre-travel prepa-
ration in order to prevent travel-related morbidity before
and after the trip.54
Perceptions of immunity and personal risk of VFRs which
may influence usage of chemoprophylaxis should be
explored, and both culturally and linguistically appropriate
information should be provided.10,57 VFRs should be
informed about the potential risks when purchasing lower
quality drugs abroad. Travel health advisors may choose less
expensive malaria prophylaxis. Policies must be reviewed to
ensure that travel-related services are accessible, afford-
able, and appropriate for these diverse populations.
Conclusions
Advance in travel medicine have been of little benefit to
VFRs, as indicated by the increasing trends of imported
malaria among them. This group of travellers is at an
increased risk for acquisition of malaria because of their
Malaria and VFRs
travel, behavioural, and cultural patterns while travelling
to their country of origin. Pre-travel services are rarely
used by VFRs. Popular beliefs that they have life-long
immunity against malaria render VFRs less likely to
receive or adhere to antimalarial chemoprophylaxis. New
strategies should be explored to approach this group of
travellers and increase awareness about malaria. Pre-travel
services should be competent, affordable, convenient and
accessible to VFRs. Medical and public health organizations
should consider new approaches to disseminate information
on travel health risks to VFRs such as community-based
campaigns in areas with large foreign-born populations.
Efforts to prevent VFRs morbidity will also contribute to
global public health.
Conflict of interest
We disclose no financial or personal relationship with other
people or organizations that could inappropriately influ-
ence our work. Both authors have made substantial
contributions to the conception and design of the article,
review and interpretation of literature, drafting of the
manuscript, and final approval of the submitted version.
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