ARTICLE IN PRESS Travel Medicine and Infectious Disease (2008) 6, 36–40
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A case of autochthonous Plasmodium vivax malaria, Corsica, August 2006 A. Armengauda,, F. Legrosb,c, E. D’Ortenziob, I. Quatresousd, H. Barree, S. Houzeb, P. Valayerf, Y. Fantonf, F. Schaffnerg a
Cellule inter re ´gionale d’e´pide´miologie sud, Marseille, France Centre National de Re´fe ´rence du paludisme, Paris and Service des Maladies Infectieuses et Tropicales, CHU Bichat, Paris, France c Institut de Recherche pour le De´veloppement, Montpellier & Paris, France d Institut de Veille Sanitaire, Saint Maurice, France e Direction de la solidarite´ et de la sante´ de Corse et de la Corse du Sud, France f Centre hospitalier d’Ajaccio, Corse du Sud, France g Entente inter de ´partementale pour la de´moustication du littoral me´diterrane´en, Montpellier, France b
Received 26 July 2007; received in revised form 20 September 2007; accepted 25 September 2007 Available online 5 November 2007
KEYWORDS Autochthonous Plasmodium vivax malaria; Corsica; France
Summary A case of Plasmodium vivax malaria was diagnosed in Corsica in summer 2006. This is the first case of autochthonous transmission of malaria to be reported in Corsica since 1972. Corsica is a well-known malaria endemic region characterised, for several years now by an anophelism situation without malaria disease, due to the presence of An. labranchiae and An. saccharovi able to transmit P. vivax. The occurring sequence of malaria signs in an imported case on 9 July and in an autochthonous case on 5 August, both in Porto, implies a transmission by local Anopheles. This suspicion is reinforced by the results of entomological investigations. However, from June to September 2006, no other P. vivax malaria case and no other autochthonous case were detected in Corsica. Therefore, it seems that no permanent malaria transmission occurs in this island. Mosquito eradication actions and anti-vectorial measures have been reinforced as well as individual prevention measures against imported diseases while travelling in tropical countries. Obviously, detection of one exceptional autochthonous transmission of one malaria case in Corsica does not justify proposing malaria protection to tourists. & 2007 Elsevier Ltd. All rights reserved.
Corresponding author. Tel.: +33 4 91 29 93 63/87; fax: +33 4 91 29 94 20.
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[email protected] (A. Armengaud). 1477-8939/$ - see front matter & 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.tmaid.2007.09.042
ARTICLE IN PRESS A case of autochthonous Plasmodium vivax malaria, Corsica, August 2006
Background An autochthonous malaria case was diagnosed in Corsica; this is the first case of autochthonous transmission of malaria to be reported in Corsica since 1972.1 In mainland France 6500–7000 imported malaria cases were reported each year between 2001 and 2004, and only rare autochthonous malaria cases were observed in airports (28 cases between 1977 and 1999) and sea ports (two cases in 1993), or by transmission via contaminated blood transfusion or tissue grafts2–4 and by contact with persons returning from endemic areas and carrying infected Anopheles in their luggage.5 Corsica is known to have been in the past endemic for Plasmodium vivax malaria and some Anopheles (Anopheles labranchiae and Anopheles sacharovi) living in the island may still have vectorial competencies for this species of plasmodium. Anti-vectorial measures are still taken and local transmission of the disease has not been observed for 35 years. Only a small number of imported cases from endemic zones are reported every year.6 Autochthonous malaria is a notifiable disease in mainland France1 and Corsica. The surveillance of imported malaria cases is based on a medical laboratories and hospitals network reporting these cases to the French National Centre for Malaria (CNR).
Materials and methods After the alert of 30 August 2006, from the Centre for Malaria which reported an alleged autochthonous P. vivax case, an epidemiological investigation was undertaken according to the recommended methodology of the CDC’s guidelines and on the basis of the following objectives7:
Checking the autochthonous status of this malaria case
documenting and detailing the disease’s transmission conditions; and Searching for other malaria cases to identify eventual local malaria transmission chain through mosquitoes in Corsica, with the aim to target anti-vectorial and mosquito eradication measures.
To reach these objectives, the following actions were decided:
Inventorying malaria cases detected from 1 June to 4
September 2006, by the Corsican medical laboratories and investigating systematically malaria P. vivax cases; Informing and alerting medical laboratories to report to the National reference centre, according to official procedures, any new case of imported or autochthonous malaria occurring after 4 September 2006, and through the mandatory notification system for the autochthonous cases; and Informing hospitals and GPs to consider this diagnosis and to report without delay suspicious autochthonous malaria
1 Notification criteria: presence of Plasmodium in thin or thick blood smears and awayness from any malaria endemic zone in the 12 months before the first symptoms.
37
cases to the medical health inspectors of the Direction of Health and Solidarity of South Corsica (DSS 2A) or of the Local Direction of Social and Sanitary Affairs of HauteCorse (Ddass 2B). In addition, an evaluation by entomological investigations, of the part of local Anopheles in the present and future transmission of Plasmodium in the local context was ordered. Species Plasmodium diagnosis was confirmed by the CNR using the standard methods (Giemsa stained blood smears) and the polymerase chain reaction (PCR)2.8
Results Epidemiological investigations The autochthonous case was a 59-year-old man living in the Department of Var, who stayed permanently this summer, from 17 June to 11 August, in the village of Porto (Department of South Corsica). On 5 August, he reported clinical symptoms including high-fever and gastro-intestinal signs and, on 11 August, was admitted to the Ajaccio hospital during 12 days where he was treated successfully with Quinimaxs (1.5 g during 5 days) for acute P. vivax malaria syndrome. The P. vivax diagnosis was confirmed by the CNR. He had never travelled into malaria endemic zones and had not been inside any airport for at least 10 years. No transfusion, no transplant or drug addiction was in his record and his last hospital admission was in 1998. On 16 June, he travelled by ferry from Toulon to Corsica to stay in the Porto area. From mid-June to 5 August, he had no clinical signs. During this stay, he was accompanied by a former military colleague (retired since 1983) who lived in Columbia and who came back to France at the end of May without any malaria record. Malaria serology by the CNR was negative for this person. Epidemiological investigations among the Corsican medical laboratories showed that another recent P. vivax case occurred in Porto. It was an imported case from Madagascar in a traveller who returned to France on 30 June 2006, and who arrived on 2 July, in Porto where he stayed permanently and where he reported, from 9 to 15 July, an acute malaria syndrome. This patient was admitted to hospital from 15 July to 23, 2006, to the Ajaccio community hospital for a primary infection and treated with Quinimaxs (1.5 g during 5 days). Then, he went back to his activities until 1 August. The diagnosis P. vivax was also confirmed by the CNR using standard and PCR methods. The sequence of these two P. vivax malaria cases in Porto, imported then autochthonous, is still an isolated phenomenon. On 26 October 2006, both prospective and retrospective investigations among the 42 Corsican medical
2
Plasmodium vivax was confirmed by the polymerase chain reaction (PCR). DNA was extracted from Giemsa stained blood smears by scrapping off each smear into a 1.5-ml microcentrifuge tube and by using the QIAamp DNA Micro Kit (Quiagen, Hilden, Germany). After amplification with specific primers,8 a 121-pb fragment compatible with Plasmodium vivax was determined.
ARTICLE IN PRESS 38
A. Armengaud et al.
Figure 1 Location of Anopheles’ breeding grounds and of both Plasmodium vivax malaria cases detected in Porto, Corsica, 2006. (Copyright & IGN Paris 2006).
laboratories3 did not show any other P. vivax malaria case in Corsica since 1 June 2006. Only rare imported malaria cases (one Plasmodium ovale and three Plasmodium falciparum) were detected by the Corsican medical laboratories. This number is within the expected range. Furthermore, in 2006, no other case of autochthonous malaria was reported through the mandatory notification disease system to the Ddass and Dss of Corsica while the CNR was not aware of any other case between June and October, 2006. Thus, these data suggest a highly probable isolated autochthonous transmission without detection of any permanent circulation of the parasite.
Entomological investigations The entomological investigations monthly undertaken in the Porto area by the anti-vectorial measures service at the Dss 2A, showed that, in the concerned area, only one breeding ground of Anopheles claviger sensu lato was found on July 27, 2006 (Figure 1). On the same day, this breeding ground was eradicated by larvicide.4 Then, on 4 September and 4 October, inquiries around the holiday residence’s case showed two breeding grounds of Anopheles petragnani, a zoophilic species and therefore considered as non-vectorial. A very few adults of the same species were numbered. In this area in July 2006, the anophelism potential seemed low and more specific to An. petragnani, without ruling out the presence of Anopheles Claviger sensu stricto (secondary historical vector in Europe)1 and, maybe, a very small number of An. labranchiae (main historical vector in Corsica).1 Introduction of infected vectors by airplanes can be excluded in Porto, considering the 30 km distance 3
On the 42 Corsican medical laboratories questioned, 29 have answered (including every laboratory carrying out parasites detection), 11 carried out Plasmodium detection tests and three identified Plasmodium between June 1 and October 26, 2006. 4 Entomological investigations, on 1 and 5 September, in the area of Porto and Girolata. Entomological report. Direction de la solidarite´ et de la sante´, Corse du Sud, September 6, 2006.
between the island’s airports. Information given by the imported case excludes the introduction of infected Anopheles from the luggage. The investigation undertaken by the Mediterranean mosquitoes eradication organisation (EID) in the area of the autochthonous case’s home in Saint-Mandrier (Var) on 5, 6, and 7 September did not show the presence of anopheles (neither adults nor larvas).2 However, the ecology of the area indicates a real Anopheles potential presence with a probable preponderance of Anopheles plumbeus species which is considered as an occasional malaria vector in Europe, and a possible presence of Anopheles Claviger s. s. In that sense, presence of autochthonous Anopheles in May and July 2006 around the case’s home cannot be completely ruled out. On the other hand, introduction probabilities of an infected vector in Saint-Mandrier are extremely low, despite the important sea traffic (especially military) in the nearby harbour of Toulon.
Management measures Advice was given to reinforce the mosquitoes’ eradication and anti-vectorial measures in Corsica as well as to improve the prevention against imported diseases, and more particularly malaria, while travelling to tropical countries to limit the number of imported cases and the risk of reintroduction of malaria to Corsica.
Discussion The occurring sequence of the malaria cases are described above, the imported case on 9 July and the autochthonous case on 5 August, both in Porto, suggests a transmission by local Anopheles. This suspicion is reinforced by the results of the entomological investigation in the Porto area and in the Department of Var. Human carriage of P. vivax gametocytes can be asymptomatic but Anopheles mosquitoes can ingest the parasites from humans carrying them without presenting acute
ARTICLE IN PRESS A case of autochthonous Plasmodium vivax malaria, Corsica, August 2006
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Figure 2 Occurring sequence of both Plasmodium vivax malaria cases detected in Porto, Corsica: one imported from Madagascar at the beginning of July and one autochthonous mid-August 2006.
malaria syndrome.9 During the first attack of malaria, this carriage of gametocytes generally follows the occurrence of clinical signs.10 Anopheles mosquitoes with P. vivax competency can be infected after biting a human being carrying gametocytes and, therefore, allow the continuation of the parasite development cycle in itself, until the presence of sporozoites in the salivary glands which can transmit the parasite to another host. In mosquitoes, the duration of the cycle (extrinsic incubation) varies from 8 to 35 days, depending on Plasmodium (Anophelian species) and weather conditions especially temperature.10 When a human is bitten by a P. vivax carried Anopheles mosquito, the duration of incubation before any clinical signs is within the average of 12–18 days (Figure 2).10 For these reasons, the occurring sequence of both P. vivax malaria cases can be compared to the dynamic of transmission by an Anopheles mosquito in the local context. However, except this isolated malaria transmission by local Anopheles, linked to the heatwave of July 2006, no other autochthonous malaria case was detected in Corsica between June and September 2006. The results of the investigation do not suggest the existence of a permanent malaria transmission chain in Corsica. In summer 1997, one autochthonous P. vivax case occurred in Italy, Department of Prevenzione. This was an autochthonous P. vivax case diagnosed in a rural zone which was known for the presence of A. labranchiae. An investigation was undertaken among 200 persons living close to the patient’s house seeking an eventual carriage of P. vivax. A malaria case imported from India 3 months before and still carrying gametocytes was detected. The entomological study did not identify the Anopheles carrying Plasmodium.11 This event linked to the summer looks like the autochthonous malaria case in Porto, Corsica, except that the imported case from Madagascar was in the primo-invasion phase and not in the chronic carriage stage of P. vivax. Other autochthonous malaria cases occurred recently in Europe: Spain in 2001 including one P. ovale autochthonous
case12 and, in summer 1997, in Germany, two P. falciparum autochthonous cases, probably transmitted by An. plumbeus, were diagnosed.13
Conclusion This first autochthonous malaria case in Corsica since 1972, following the P. vivax malaria case imported from Madagascar in July 2006 to Porto, was not really an isolated phenomenon since other European countries have documented recently this risk.11–13 This was a warning which demonstrated that mosquito eradication and anti-vectorial measures should be maintained and reinforced in Corsica especially during heatwaves. In addition, individual health advice against imported diseases for travellers to tropical countries should be improved in Corsica in order to avoid the creation of a human reservoir of the parasite which might infect local Anopheles mosquitoes.2,6,14–16 In the same way, systematic use of anti-gametocyte treatment for P. vivax acute malaria crisis in Corsica should be considered. However, the detection of one exceptional malaria infection transmitted by mosquitoes in Corsica does not justify suggesting malaria protection for residents and tourists in Corsica.
Acknowledgements Cellule inter re´gionale d’e´pide´miologie sud, Marseille: S. Cano, P. Malfait. Centre National de Re´fe ´rence du paludisme, Paris: V. Hubert, J. Le Bras, M. Danis. Institut de Recherche pour le De´veloppement, Montpellier: D. Fontenille. Institut de Veille Sanitaire, Saint Maurice: A. Tarantola. Centre hospitalier d’Ajaccio, Corse du Sud: D. Bertei.
ARTICLE IN PRESS 40 Direction de la solidarite´ et de la sante´ de Corse et de la Corse du Sud, Ajaccio: C. Maury, Fx. Pernice, P. Maroselli, J.L. Wyart, A. Macarry. Direction ge ´ne´rale de la Sante´, Paris: E. Falip, M. Baville, B. Faliu. L’ensemble des laboratoires de biologie et d’analyses me ´dicales de Corse.
References 1. Guillet P. Paludisme, lutte anti-vectorielle et de ´moustication en Corse. Rapport de mission-Aou ˆt 1996-ORSTOM, 1996. p. 1–28. 1996. 2. Legros F, Arnaud A, El Mimouni B, Danis M. Paludisme d’importation en France me ´tropolitaine: donne´es e´pide ´miologiques, /http://www.invs.sante.fr/beh/2006/32/beh_32_2006.pdfS; 2001–2004. 3. Lusina D, Legros F, Esteve V, Klerlein M, Giacomini T. Airport malaria: four new cases in suburban Paris during summer 1999. Euro Surveill 2000;5(7):76–80. 4. Delmont J, Brouqui P, Poullin P, Pouymayou C, Faugere B, Ottomani A, et al. Apropos of 2 cases of severe malaria contracted in the port of Marseille. Bull Soc Pathol Exot 1995;88(4):170–3. 5. Giacomini T, Gougal H, Boudon P, Rennes C, Dumouchel P, Petithory JE. Two cases of falciparum malaria. Probable responsibility of Anopheles transported by air. Bull Soc Path Exot 1977;70(4):375–9. 6. Gourvellec G, et al. Surveillance du paludisme en Corse, /http://www.invs.sante.fr/publications/2005/paludisme_corse/ index.htmlS; 1999–2002.
A. Armengaud et al. 7. CDC. Locally acquired mosquito-transmitted malaria: a guide for investigations in the United States, /http://www.cdc.gov/ mmwr/PDF/rr/rr5513.pdfS. 8. Snounou G. Detection and identification of the four malaria parasite species infecting humans by PCR amplification. Methods Mol Biol 1996;50:263–91. 9. Nacher M, Silachamroon U, Singhasivanon P, Wilairatana P, Phumratanaprapin W, Fontanet A, et al. Risk factors for Plasmodium vivax gametocyte carriage in Thailand. Am J Trop Med Hyg 2004;71(6):693–5. 10. Heymann DL. Control of communicable diseases manual, 18th ed. American Public Health Association; 2004. p. 324–340. 11. Baldari M, Tamburro A, Sabatinelli G, Romi R, Severini C, Cuccagna G, et al. Malaria in Maremma, Italy. Lancet 1998; 351(9111):1246–7. 12. Cuadros J, Calvente MJ, Benito A, Arevalo J, Calero MA, Segura J, et al. Plasmodium ovale malaria acquired in central Spain. Emerg Infect Dis 2002;8:1506–8. 13. Kru ¨ger A, Rech A, Su X-Z, Tannich E. Two cases of autochthonous Plasmodium falciparum malaria in Germany with evidence for local transmission by indigenous Anopheles plumbeus. Trop Med Int Health 2001;6:983. 14. Recommandations sanitaires pour les voyageurs 2006 (a ` l’attention des professionnels de sante´), /http://www.invs. sante.fr/beh/2006/23_24/beh_23_24_2006.pdfS. 15. Recommandations sanitaires aux voyageurs, Institut de veille sanitaire, /http://www.invs.sante.fr/display/?doc=presse/2004/ le_point_sur/recommandations_voyageurs/index.htmlS. 16. Informations sur la pre ´vention et le traitement des maladies tropicales et des affections lie ´es au voyage, Ministe `re de la Sante ´ et des Solidarite ´s, /http://www.sante.gouv.fr/htm/ pointsur/voyageurs/sommaire.htmS.
