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Dispatch
Malaria Clusters among Illegal
Chinese Immigrants to Europe through Africa
Zeno Bisoffi,* Alberto Matteelli,† Donatella Aquilini,‡ Giovanni Guaraldi,§
Giacomo Magnani,¶ Giovanna Orlando,# Giovanni Gaiera,** Tomas Jelinek,††
and Ron H. Behrens‡‡
*Ospedale S. Cuore, Negrar, Verona, Italy; †Università di Brescia, Brescia,
Italy; ‡Ospedale di Prato, Prato, Italy; §Università di Modena, Modena,
Italy; ¶Ospedale di Reggio Emilia, Reggio Emilia, Italy; #Ospedale Sacco,
Milano, Italy; **Ospedale S. Raffaele, Milano, Italy; ††Institute of Tropical
Medicine, Berlin, Germany; and ‡‡London School of Hygiene and Tropical
Medicine, London, United Kingdom
Suggested citation
for this article:
Bisoffi Z, Matteelli A, Aquilini D, Guaraldi G, Magnani G, Orlando G,
et al. Malaria clusters among illegal Chinese immigrants to Europe through
Africa. Emerg Infect Dis [serial online] 2003 Sep [date cited].
Available from: URL: http://www.cdc.gov/ncidod/EID/vol9no9/03-0353.htm
Between November
2002 and March 2003, 17 cases of malaria (1 fatal) were observed in
illegal Chinese immigrants who traveled to Italy through Africa. A further
cluster of 12 was reported in August, 2002. Several immigrants traveled
by air, making the risk of introducing sudden acute respiratory syndrome
a possibility should such illegal immigrations continue.
From November 2002 to March 2003, 17 cases of malaria were noted among
illegal Chinese immigrants in seven hospitals across central and northern
Italy (15 cases of Plasmodium falciparum, 1 case of P. malariae,
and 1 mixed infection of P. falciparum and P. malariae).
One patient died. Until recently, imported malaria in this group of illegal
immigrants from China was not detected by malaria surveillance institutions
within Europe (1). Although malaria is still endemic
in parts of China, transmission in these regions is low-level (2);
the predominant species is P. vivax. P. falciparum transmission
is confined to provinces bordering Laos and Viet Nam. None of the patients
reported coming from those areas. Investigating the cluster proved difficult
because of language problems and reticence to provide detailed information
of travel, since the patients were illegal immigrants (Table).
The fatal case occurred in a general hospital in northern Italy. The 20-year-old
woman (case 7) was admitted with a high fever, severe hemolytic anemia
(hemoglobin 4.4 g/dL), and metabolic acidosis. After 48 hours, because
of hypotension, seizures, and subsequent coma, she was transferred to
the intensive-care unit of a referral hospital for infectious diseases.
The blood film showed a 70% parasitemia with P. falciparum. The
patient died 96 hours after admission, despite aggressive drug therapy
and plasmapheresis.
Discussion
Before 2000, no cases of P. falciparum had occurred in Chinese
immigrants living in northern and central Italy, despite a large immigrant
population. An initial cluster of 22 cases was described during summer
2000 in the Lombardy Region (3). A cluster of six cases
was detected in Tuscany during the same period (4). In
both outbreaks, the researchers described high rates of severe disease.
All patients were exposed to malaria during a prolonged journey to Europe
(3–9 months) through a number of Asian and African countries.
From 2000 to 2002, a total of 10 sporadic cases were reported to the
Italian Ministry of Health in 2001 (L. Vellucci, Directorate for Prevention,
Ministry of Health, Italy, pers. comm.). The 2003 cluster prompted us
to examine hospital records from August 2002, where we identified an additional,
previously undetected, cluster of 12 malaria cases in four of our study
hospitals (data not included in the table). The Ministry
of Health had 26 confirmed P. falciparum cases during 2002 (L.
Vellucci, pers. comm.), suggesting an ongoing (and possibly increasing)
influx of Chinese laborers. Some differences exist between the later cluster
and the 2000 cluster. In the 2003 cluster, the proportion of severe cases
was lower than in the previous reports, with a patient with a fatal case
first admitted to a general hospital where diagnosis of malaria was not
considered; in the others, awareness of the possibility of malaria had
been raised by the earlier cluster (3,4) and led to prompt
diagnosis and treatment, with favorable outcome. A single African country,
Côte d’Ivoire, was the transit country for most of the patients. In previous
cases, a number of other African countries were used for transit. Visa
processing for entry to Europe was arranged by the courier organization
in Côte d’Ivoire. The clustering of cases suggests that the illegal immigrants
arrive in Europe in groups. Although Italy was the final destination,
at least some immigrants entered through France, which also has had reports
of P. falciparum cases in Chinese immigrants (F. Legros, Centre
National de Référence de l’Epidémiologie du Paludisme, France, pers. comm.).
As malaria is probably underreported in Europe, additional cases may well
have occurred.
Use of clandestine travel by air to emigrate from China, where sudden
acute respiratory syndrome (SARS) is present, poses a threat for the African
countries, where the introduction of SARS virus could have devastating
consequences on their health systems with a potential overlap with the
HIV epidemic. Other diseases could be spread or acquired by the immigrants
in the countries of transit. While curtailing the huge, illegal immigrant
system to Europe is difficult, we cannot overemphasize the need for a
sound surveillance on imported infectious diseases in this continent.
Both clusters of malaria were detected early through Salute Internazionale
Regione Lombardia (SIRL), a network on imported diseases of the Lombardy
Region, in conjunction with the European Network on Imported Infectious
Disease Surveillance (TropNetEurop). Any physician in Europe who sees
a Chinese patient with a history of recent travel and a high fever should
exclude malaria, besides considering the possible diagnosis of SARS. Respiratory
symptoms are also frequent in uncomplicated malaria (5,6),
and acute respiratory distress syndrome has long been recognized as one
of the main features of severe malaria (7,8).
Acknowledgments
We are grateful
to Loredana Vellucci, Stefania D’Amato, and Fabrice Legros for providing
information on malaria in Chinese immigrants in Italy and France, respectively.
Dr. Bisoffi is the
head of the Center for Tropical Diseases at the Sacro Cuore Hospital
of Negrar, Verona, Italy, a referral center for imported diseases. His
main research interests concern the surveillance and diagnosis of imported
tropical and infectious diseases and the clinical decision-making in
tropical medicine. He is the secretary general of the Italian Society
of Tropical Medicine and teaches in several Italian and European institutes.
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Table.
Characteristics of 17 cases of malaria in illegal Chinese immigrants,
Italy |
|
Case |
Sex, agea
|
Date first seen
by physician
|
Country of transit
|
Time spent in
country of transit
|
Mode of travel
|
Mode of travel
to Europe
|
Plasmodium species
|
Clinical outcome
|
|
1
|
M, 21
|
11/05/02
|
Côte d’Ivoire
|
8 mo
|
Air
|
Air
|
P. falciparum
|
Recovered
|
2
|
M, 24
|
11/11/02
|
“Africa”
|
3 mo
|
Unknown
|
Air
|
P. falciparum
|
Recovered
|
3
|
F, 20
|
11/12/02
|
Côte d’Ivoire
|
22 d
|
Road/sea
|
Air
|
P. falciparum
|
Recovered
|
4
|
M, 22
|
11/15/02
|
Côte d’Ivoire
|
1 mo
|
Air
|
Air
|
P. falciparum
|
Recovered
|
5
|
M, 24
|
11/16/02
|
Côte d’Ivoire
|
14 d
|
Road/sea
|
Air
|
P. falciparum
|
Recovered
|
6
|
M, 28
|
01/09/03
|
Côte d’Ivoire
|
2 mo
|
Unknown
|
Air
|
P. falciparum
|
Recovered
|
7
|
F, 20
|
01/13/03
|
Côte d’Ivoire
|
Few days
|
Unknown
|
Air
|
P. falciparum
|
Died
|
8
|
M, 21
|
02/01/03
|
Côte d’Ivoire
|
Unknown
|
Unknown
|
Air
|
P. falciparum
|
Recovered
|
9
|
F, 32
|
02/02/03
|
Congo
|
Unknown
|
Unknown
|
Air
|
P. falciparum
|
Recovered
|
10
|
M, 22
|
02/03/03
|
Côte d’Ivoire
|
6 mo
|
Air
|
Air
|
P. falciparum
|
Recovered
|
11
|
M, 19
|
02/08/03
|
Côte d’Ivoire
|
Unknown
|
Unknown
|
Air
|
P. falciparum
|
Recovered
|
12
|
M, 34
|
02/13/03
|
Congo
|
2 mo
|
Road/sea
|
Air
|
P. falciparum and
P. malariae
|
Recovered
|
13
|
F, 24
|
02/13/03
|
Côte d’Ivoire
|
50 d
|
Air
|
Air
|
P. falciparum
|
Recovered
|
14
|
M, 40
|
02/22/03
|
Côte d’Ivoire
|
Unknown
|
Road/sea
|
Air
|
P. falciparum
|
Recovered
|
15
|
M, 22
|
02/24/03
|
Côte d’Ivoire
|
2 mo
|
Road/sea
|
Air
|
P. falciparum
|
Recovered
|
16
|
M, 28
|
03/01/03
|
“Africa”
|
Unknown
|
Unknown
|
Air
|
P. falciparum
|
Recovered
|
17
|
M, 23
|
03/15/03
|
Côte d’Ivoire
|
50 d
|
Road/sea
|
Air
|
P. malariae
|
Recovered
|
|
aM, male; F, female. |
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