Origin and prevention of airport malaria in France

Article (PDF Available)inTropical Medicine & International Health 3(9):700-5 · October 1998with84 Reads
DOI: 10.1046/j.1365-3156.1998.00296.x · Source: PubMed
Abstract
Since 1969, 63 cases of airport malaria have been reported in Western Europe, 24 of which occurred in France. Most were due to Plasmodium falciparum. In 1994, 7 cases occurred in and around Roissy Charles de Gaulle airport (CDG), showing 4 types of contamination: among employees working on airstrips or opening containers, among residents living near the airport, among people living at some distance from the airport after a secondary transport of vectors, and by vectors transported in luggage. In-flight or stop-over infection is not considered as airport malaria. The infective anophelines originated from airports where malaria transmission occurs, mostly in subsaharan Africa. A tentative list is given taking into account aerial traffic with France. Surveys in the airports of Dakar (Senegal), Cotonou (Benin), Abidjan (Cote d'Ivoire) and Yaoundé (Cameroun) found potential vectors in all of these from July to September. After 1994, the Contrôle Sanitaire aux Frontières (CSF) in charge at CDG concentrated its efforts on the flights at risk, as well as information and sensitization of airline companies, which resulted in 73% and 87% of the flights at risk being properly disinsected in 1995 and 1996. Despite pyrethroid resistance in Anopheles gambiae s.s. in West Africa, the efficacy of aircraft spraying with permethrin aerosols is still acceptable. However, surveillance of resistance should be improved and search for nonpyrethroid insecticides suitable for aircraft strongly encouraged.
Tropical Medicine and International Health
volume 3 no 9 pp 700–705 september 1998
© 1998 Blackwell Science Ltd
700
Origin and prevention of airport malaria in France
P. Guillet
1
, M. C. Germain
2
, T Giacomini
3
, F. Chandre
1
, M. Akogbeto
4
,O.Faye
5
, A. Kone
6
, L. Manga
7
& J. Mouchet
8
1 ORSTOM-LIN, Montpellier, France
2 DDASS Seine St Denis, Contrôle Sanitaire aux Frontières, France
3 Centre Hospitalier Robert Balanger, Aulnay-sous-Bois, France
4 Centre de Recherches Entomologiques, Cotonou, Benin
5 Laboratoire de Paludologie, Université de Dakar, Senegal
6 Institut National d’Hygiène Publique, Abidjan, Côte d’Ivoire
7 OCEAC Yaoundé Laboratoire de Lutte Antivectorielle, Cameroun
8 ORSTOM, Paris, France
Summary Since 1969, 63 cases of airport malaria have been reported in Western Europe, 24 of which occurred in
France. Most were due to Plasmodium falciparum. In 1994, 7 cases occurred in and around Roissy Charles de
Gaulle airport (CDG), showing 4 types of contamination: among employees working on airstrips or opening
containers, among residents living near the airport, among people living at some distance from the airport
after a secondary transport of vectors, and by vectors transported in luggage. In-flight or stop-over infection
is not considered as airport malaria. The infective anophelines originated from airports where malaria
transmission occurs, mostly in subsaharan Africa. A tentative list is given taking into account aerial traffic
with France. Surveys in the airports of Dakar (Senegal), Cotonou (Benin), Abidjan (Cote d’Ivoire) and
Yaoundé (Cameroun) found potential vectors in all of these from July to September. After 1994, the Contrôle
Sanitaire aux Frontières (CSF) in charge at CDG concentrated its efforts on the flights at risk, as well as
information and sensitization of airline companies, which resulted in 73% and 87% of the flights at risk
being properly disinsected in 1995 and 1996. Despite pyrethroid resistance in Anopheles gambiae s.s. in West
Africa, the efficacy of aircraft spraying with permethrin aerosols is still acceptable. However, surveillance of
resistance should be improved and search for nonpyrethroid insecticides suitable for aircraft strongly
encouraged.
keywords Airport malaria, Plasmodium falciparum, pyrethroids, sub-Saharan Africa
correspondence: Dr P Guillet, ORSTOM-LIN, BP 5045, 34032 Montpellier Cedex 1, France
Introduction
The first cases of airport malaria in France were
retrospectively diagnosed in 1969 in Le Bourget Airport, 6 km
north of Paris (Doby & Guiguen 1981). Since then, 24 cases
were recorded in France and 41 in the rest of western Europe
(Belgium, Italy, the Netherlands, Spain, Switzerland and
United Kingdom). A list of these cases was compiled by
Giacomini et al. (1995), updated in 1996 by Dr P. Carnevale
(unpublished observations) and in 1997 by our team. All
cases were due to Plasmodium falciparum except one case of
P. malariae in Switzerland (Giacomini et al. 1995) and one
doubtful case of P. vivax in France (Larcan et al. 1978). Most
cases were recorded during the summer and only 3 occurred
during the winter and were luggage malaria.
In 1994, 7 cases of P. falciparum malaria were recorded
among non-travelling people in and around Roissy-Charles-
de-Gaulle (CDG), the main airport serving tropical Africa.
An immediate epidemiological survey with an entomological
component confirmed that they were airport malaria. Further
research in 1995 established the possible origin of infective
vectors (anopheline mosquitoes), assessed the efficacy of
aircraft disinfection procedures and controlled their
application by airline companies. The overall objective was to
propose practical measures to prevent airport malaria.
Sites and ways of contamination
The first step was to make sure that there were no vectors in the
vicinity of the airport able to transmit P. falciparum.
Indigenous anophelines in and around airports of western
Europe ] Anopheles messae, A. atroparvus and A. labranchiae
TMIH296
Tropical Medicine and International Health volume 3 no 9 pp 700–705 september 1998
P. Guillet et al. Origin and prevention of airport malaria in France
(the latter occurs only in Italy) ] were shown to be refractory to
P. falciparum (Ramsdale & Coluzzi 1975). Another common
species, A. claviger, has never been associated with malaria.
However, as the 1994 summer was very hot, it was
hypothesized that imported tropical anophelines such as A.
gambiae s.l. could temporary breed in local water pools.
Examination of potential breeding sites in the vicinity of
reported cases gave no proof supporting this hypothesis.
Obviously cases in and around the airport were transmitted by
infective anophelines imported by aircraft. Once infective
mosquitoes arrive in an airport, they can disseminate the
parasite in different ways.
Transmission inside the airport
Ground personnel working on airstrips are at risk when the
cabin and cargo hold doors are opened. Also, those who
manipulate and open containers in warehouses, stores or the
post office are exposed to bites of the vectors which have
travelled in containers. In 1994, three cases were recorded
among airstrip personnel and two among container
manipulators, including a mailman (Giacomini et al. 1995).
Transmission among the airport nearby residents
Nearby residents are also exposed to bites of mosquitoes
coming from the airport. Two cases in 1969 and one in 1995
were reported near Le Bourget airport, and three cases near
CDG in 1976, 1977 and 1987 (Giacomini et al. 1977, 1988).
Transmission after a second transport of the vector
Two cases occurred among people living in an urban area
located 7 km away from the airport, who had no contact with
any airport and never travelled to endemic areas. However, a
number of airport employees lived in the immediate vicinity.
The only reasonable explanation was that anophelines were
brought by car by airline employees. Interviews with the
employees revealed that at the time they were on night shift and
their cars were parked near airstrips. The CO
2
emitted by the
engine when a car is starting can attract mosquitoes.
Similar cases of secondary transport over several kilometres
were reported in England (Whitfield et al. 1984) and Italy (Rosci
et al. 1987).
Luggage malaria
Luggage has often been suspected of harbouring mosquitoes,
possibly causing infections when opened at arrival. Such cases
were reported in Italy in 1989 (luggage loaded in Benin) (Rizzo
et al. 1989) and France in 1995 (luggage loaded in Haiti) (Dr T.
Giacomini, unpublished observation).
In-flight infection
There is evidence of a passenger having been infected during a
flight from Johannesburg to Paris which stopped over at
Abidjan airport, where the aircraft doors were left open
(Conlon et al. 1990). As there is no malaria in Johannesburg,
the infected anophelines evidently got on board at Abidjan.
Another case was a serviceman supposedly infected during a
night stop-over at Banjul, The Gambia. These cases do not
meet the definition of airport malaria.
Possible origin of infective anophelines
Tentative list of airports at risk
To focus the activities of sanitary control on flights at risk of
introducing infective vectors, we tried to establish a list of
airports where infective mosquitoes are likely to get on board.
About 100 countries are considered malarious by the WHO
(1995), but only a limited number of airports are at risk, i.e.
located within an area where P. falciparum is actively
transmitted. A flight is considered at risk when it lands at one
of these airports
Most international airports of Asia and the Americas are
located in areas where there is no P. falciparum transmission
even if the country is classified as malarious. This is the case in
Hanoi and Ho Chi Minh in Vietnam; Phnom Penh in
Cambodia; Bangkok in Thailand; Sao Paulo, Rio de Janeiro
and Brasilia in Brazil, for example. Moreover, some airports
implemented effective vector control measures as recommended
by international legislation.
In establishing a list of airports at risk, we have not
considered countries without direct connections with France
(e.g. Papua-New Guinea), and for a more complete list, the
increasing number of charters, military and cargo flights need
to be considered also.
So far, most cases were recorded in summer (July usually
being the warmest month in western Europe) and
predominantly in very warm years (Figure 1). Apart from the
warm temperatures which favour anopheline activity, European
summertime corresponds to the rainy season in tropical
countries of northern hemisphere, the peak of mosquito
production and malaria transmission. According to these
criteria and taking into account the traffic in French airports,
we propose a tentative list of airports at risk, which should be
periodically updated and completed.
West Africa
Benin (Cotonou), Burkina-Faso (Ouagadougou), Côte d’Ivoire
(Abidjan), Guinea (Conakry), Mali (Bamako), Niger (Niamey),
Nigeria (Lagos, Kaduna, Kano), Senegal (Dakar), Togo (Lome).
At the moment, there are no direct flights to France from
Guinea Bissau, The Gambia, Ghana, Liberia and Sierra Leone.
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Central, East and Southern Africa
Cameroun (Douala, Yaoundé), Chad (Ndjamena), Djibouti,
Central African Republic (Bangui), Gabon (Libreville), the
Congo (Brazzaville), Congo DM (Kinshasa), Kenya (not
Nairobi but charters from Mombasa), Sudan (Khartoum),
Uganda (Entebbe), Angola (Luanda), Comoro Islands
(Moroni), Zambia (Lusaka), Mozambique (Maputo),
Madagascar (not Antananarivo but charters from Nosy-Be).
Americas
Haiti (Port-au-Prince).
In France, most flights at risk arrive at CDG, Paris, and to a
much lesser extent at Marseille, Nice, Lyon, Bordeaux and
Toulouse. Charters and private flights land at Le Bourget and
Orly. Military airfields such as Frejus, Istres and Villacoublay
should also be considered. European airports with many
connections to Africa had the greatest number of malaria
cases: France (24 cases), Belgium (16), Switzerland (10), UK
(4), whereas those with fewer links recorded fewer cases: Italy
(4), Germany (2), The Netherlands (2), Spain (1).
Entomological research studies in airports of tropical Africa
To support our hypothesis of an African origin of infective
mosquitoes, entomological surveys were carried out in the
airports of Dakar (Senegal), Abidjan (Côte d’Ivoire),
Cotonou (Benin) and Yaoundé (Cameroun) from July to
September 1995. In the last three countries where four
seasons occur, rainfall is high in July but decreases in August
and September (minor dry season) along with anopheline
densities. However, transmission is almost perennial. The
results (Tables 1 and 2) were as follows:
In Dakar, two people did one-night collections every two
weeks from July to November, both inside and outside the
airport. Anopheles arabiensis was found only in August (2)
and September (5). Five A. pharoensis and 2720 Culex
quinquefasciatus were harvested.
In Abidjan, 12 night/man collections (4 per month)
harvested 54 A. gambiae s.s., 38 in July, 15 in August, 1 in
September. Twenty-nine were caught on the airstrip (near the
aircraft) and 25 in the luggage container-loading area.
23
14
1969
Year
Temperature °C
18
22
21
20
19
17
16
15
1971 1973 1975 1977 1979 1981 1983 1985 1987 1989 1991 1993 1995
Figure 1 Average July temperature in 4
western European airports. h Paris;
j Brussels; d Geneva; s London.
Ta b l e 1 Number of malaria vectors and other mosquito species collected in 4 international airports in Africa, July September 1995
Dakar Abidjan Cotonou Yaoundé
——————————— ——————————— ——————————— ———————————
Night/ Malaria Other Night/ Malaria Other Night/ Malaria Other Night/ Malaria Other
Month man vectors species man vectors species man vectors species man vectors species
July 2 00218085 0215
August 2 01226083 0414
September 2 010 2 11 080 04 08
Total 6 11 2780 6 55 297 24 8 193 10 37 2
Tropical Medicine and International Health volume 3 no 9 pp 700–705 september 1998
P. Guillet et al. Origin and prevention of airport malaria in France
In Cotonou at 24 night/man collections around aircraft
flying to Roissy, 8 A. gambiae s.l were collected together with
193 C. quinquefasciatus. In 24 luggage containers inspected,
2 A. gambiae were caught. Larval sites of A. gambiae s.l.
were numerous in the area in July but dried out in August.
In Yaoundé, 5 A. gambiae s.s. (all in July), 2 A. funestus
and 28 A. moucheti were collected in 10 night/man
collections. The latter species, a very good vector in the area,
is not rainfall-dependent because it breeds in rivers. No
mosquitoes were found during night surveys in a Boeing 737
parked on the tarmac with open doors. It is important to note
that in a village at the edge of the airport the sporozoitic
index was 2.5% for A. gambiae s.s. and 1.7% for A. moucheti
(Manga et al. 1995).
Most of the anophelines collected were dissected but no
sporozoite was found in the salivary glands and the search for
circumsporozoite antigen by ELISA was also negative.
However, the number of dissected anophelines (, 50) was
too low to draw any conclusion. Parous rates were over 50%,
which is consistent with the possibility of transmission. It is
interesting although not surprising that no anopheline was
found in aircraft parked on the tarmac at night, because there
was neither bait nor any attractant in the empty plane. It is
likely that anophelines enter a plane with passengers or are
attracted by the C0
2
emitted by the power units before take-
off, when cabin and cargo hold are still open. Many flights
take off after 10 p.m., which corresponds to the peak activity
of A. gambiae s. l. The two A. gambiae females found inside
containers in Cotonou were bloodfed, i.e. they were resting in
the containers during their blood meal digestion.
Prevention of airport malaria
According to international sanitary regulations, the area of
airports themselves and the perimeter of 400 m around the
airport must be made free of Aedes aegypti and malaria
vectors. However, vectors were found in all airports suspected
to be at the origin of cases, whether they had mosquito
control or not. Beside these measures, all aircraft coming
from endemic areas must be disinsected before landing in
nonendemic areas. The application of instructions varies
from country to country. In France, emphasis is mainly on
control of malaria, plague and ] to a lesser extent ]
haemorrhagic fever vectors. Aircraft disinsection guidelines
proposed by the WHO are based on the use of pyrethroids
(either aerosols or residual treatment) and were recently
reviewed (WHO 1985, 1995). The efficacy of these procedures
was assessed within the framework of our study and will be
published separately.
Organization of control in France
Airport controls are the responsibility of the Contrôle
Sanitaire aux Frontières (CSF), a branch of the Direction
Départementale des Affaires Sanitaires et Sociales (DDASS).
Until 1994, all flights coming from endemic areas were
eligible for control according to the list of malaria countries
provided by WHO (103 countries). But due to the great
number of flights involved, controls were random and on a
small proportion of aircraft only. Immediately after the 1994
cases, we alerted the sanitary authorities to the necessity of
more exhaustive controls of flights at risk.
Action at level of airline companies
The implementation of disinsection procedures
recommended by WHO is the responsibility of airline
companies. Aircraft are supposed to be disinsected before
opening their doors upon arrival. In case of control by CSF,
empty cans used in cabin and cargo (in case of aerosol
disinfection) or a certificate of residual treatment must be
presented by the cabin crew to the health officer.
At the end of 1994 and in 1995 the health authorities held
meetings with airlines to make the companies aware of the
danger of vector importation and to remind them of French
disinsection rules. Most airlines responded favourably and
were acquainted with the legislation although it was not
always applied. Scientists attending the meeting drew
attention to flights most at risk.
Results of aircraft control
The results of CSF controls of landing aircraft are
summarized in Table 3. Priority was given to flights from
West and Central Africa. The percentage of infractions
significantly decreased from June to September 1995 (58]8%)
following enforcement of controls of flights at risk. In 1996,
overall infractions accounted for only 13% compared to 26%
in 1995. No information about the situation of cargo or
military aircraft was available.
© 1998 Blackwell Science Ltd
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Ta b l e 2 Collection areas for adult malaria vectors in four
international airports in Africa, July September 1995
Collection area
————————————————————
Luggage Inside
Airport Tarmac loading area luggage container
Dakar 04 07 Not inspected
Abidjan 29 26 Not inspected
Cotonou 03 052
Yaoundé 7 30 Not inspected
Tropical Medicine and International Health volume 3 no 9 pp 700–705 september 1998
P. Guillet et al. Origin and prevention of airport malaria in France
The most common infraction was non-disinsection of
cargo hold (48%) and cabin (13%), inadequate quantity of
aerosols (18%) and incomplete forms (12%). This varied
greatly according to airline companies, the highest
proportion was recorded among small airlines operating only
one or two aircraft.
There were no cases of airport malaria reported in CDG in
1995, 1996 and 1997 when sanitary controls focused on flights
at risk and aircraft were better disinsected. One doubtful case
of luggage malaria coming from Haiti was reported in 1995.
A second case (Giacomini, personal observation) concerned a
child infected in a house near Le Bourget airport, which
receives only private flights. These are almost impossible to
control efficiently because most flights are not scheduled.
During the same period, 8 cases were recorded in Brussels.
Discussion and conclusion
In western Europe, the trends of average temperature in July
are the same in all countries, but year-to-year differences can
exceed 3 8C (Figure 1). From 1969 to 1996, airport malaria
cases were reported in 20 years. It is almost impossible to
correlate its occurrence with temperature because the number
of cases is too small. However, no case was observed during
the coolest years. In London, where the average temperature
in July is lowest (Figure 1), four cases were reported in 1983
(Warhust et al. 1984), one of the warmest summers in the 27
years considered. Taking into account these figures, it is
reasonable to infer that the risk of airport malaria as greater
during warm years.
Epidemiological as well as entomological investigations
have highlighted the role of containers in the transport of
vectors. Possible cases of luggage malaria have been reported
in Italy and suspected in France; however, further
investigations are needed. For cases occurring far away from
the airport, the probability of misdiagnosis is high. Whatever
disinsection procedure is used, it is likely that vectors inside
luggage escape treatment. Secondary transport of vectors
from the airport should also be considered, although if the
plane was properly disinsected this ought not to occur.
With the discovery of resistance to pyrethroids in A.
gambiae s.s. from Côte d’Ivoire (Elissa et al. 1993), doubts
arose about the efficacy of aircraft disinsection procedures
with pyrethroids. We have found that, despite resistance,
aerosol sprays were still acceptable (over 80% control
compared to 100% with susceptible mosquitoes of this
species) (Dr P. Guillet et al. unpublished observation). But the
possibility for an increase of pyrethroid resistance exists
which would make the current disinsection procedures
useless. For example, it was observed that highly resistant
Culex quinquefasciatus travels almost unharmed in treated
aircraft. A surveillance program on the evolution of
pyrethroid resistance among malaria and other disease
vectors is necessary. As pyrethroids are the only insecticides
currently available for aircraft disinsection, there is an urgent
need to reactivate the search for an alternative.
After the 7 cases reported in 1994 in CDG, was proposed to
classify flights with regard to risk of carrying infective
malaria vectors. The malaria situation in endemic countries
should be evaluated in the vicinity of the international
airports and not at country level. With a precise and up-to-
date classification of risks, disinsection can be effective,
placing minimal constraints on airlines, cabin crew,
passengers and sanitary services.
According to WHO, the malaria situation is deteriorating
throughout the world, but especially in Africa, with an
increasing risk of infected vectors entering aircraft.
Consequently, thorough information and sensitization of
airline companies as well as effective sanitary controls in
international airports are mandatory. Transport of malaria
vectors is only one particular case of the more general
problem of dissemination of vectors (Mouchet et al. 1995;
Rhodain 1996) and agricultural pests together with the
pathogens and resistance genes they carry. As most European
countries are concerned, it would be desirable to harmonise
at EC level policies both on aircraft disinsection and sanitary
control.
© 1998 Blackwell Science Ltd
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Ta b l e 3 Control of aircraft landing at Roissy airport and observance of disinsection procedures by airline companies
June July August September Total
1995
Controls 38 81 69 50 238
Infractions 22 (58%) 22 (27%) 14 (20%) 04 (8%) 062 (26%)
1996
Controls 43 58 39 22 162
Infractions 02 (4.7%) 12 (20.7%) 05 (12.8%) 04 (18.2%) 023 (14.2%)
Tropical Medicine and International Health volume 3 no 9 pp 700–705 september 1998
P. Guillet et al. Origin and prevention of airport malaria in France
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    Full-text · Article · Jan 2016 · Malaria Journal
    • "The infected female mosquito leaving the aircraft, can survive long enough and can be dispersed under wind conditions from 7 to 15 km [16,17] . It could be transported further by vehicle and baggage [18,19]. Genotyping of the four P. falciparum isolates obtained from patients showed that a similar strain was involved. "
    [Show abstract] [Hide abstract] ABSTRACT: Four cases of airport malaria were notified for the first time in Tunisia during the summer of 2013. All patients were neighbours living within 2 km of Tunis International Airport. They had no history of travel to malarious countries, of blood transfusion or of intravenous drug use. Although malaria transmission had ceased in Tunisia since 1980, autochthonous infection by local Anopheles mosquitoes was initially considered. However, this diagnostic hypothesis was ruled out due to negative entomological survey and the absence of additional cases. All cases were caused by Plasmodium falciparum. Clinical presentation was severe (important thrombocytopaenia and parasitaemia), because of relatively important delay in diagnosis (average of seven days). This indicates the need to consider malaria while examining airport employees or people living near international airports presenting with fever of unknown origin. It also stresses the need for effective spraying of aircrafts coming from malarious areas.
    Full-text · Article · Jan 2015
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