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Systematic Review Open Access
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Abstract

Background

Airport and luggage (also called Odyssean) malaria are chance events where infection results from the bite of an infected mosquito which was transported by aircraft from a malaria-endemic area. Infrequent case reports and a lack of central data collection challenge a comprehensive overview.

Aim

To update the epidemiological, clinical and biological understanding of airport and luggage malaria cases in Europe.

Methods

We conducted a systematic review of studies indexed from 1969 to January 2024 in MEDLINE, Embase and OpenGrey databases. A data call to EU/EEA and UK public health institutes was launched in December 2022.

Results

Of the 145 cases (89 cases from 48 studies and 56 cases from the data call) described from nine countries, 105 were classified as airport malaria, 32 as luggage malaria and eight as either airport or luggage malaria. Most airport malaria cases were reported in France (n = 52), Belgium (n = 19) and Germany (n = 9). Half of cases resided or worked near or at an international airport (mean distance of 4.3 km, n = 28). Despite disruptions in air travel amid the COVID-19 pandemic, one third of cases reported since 2000 occurred between 2018 and 2022, with a peak in 2019.

Conclusion

While airport and luggage malaria cases are rare, reports in Europe have increased, highlighting the need for effective prevention measures and a more structured surveillance of cases in Europe. Prevention measures already in place such as aircraft disinsection should be assessed for compliance and effectiveness.

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2024-10-10
2024-11-13
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.41.2400237
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References

  1. European Centre for Disease Prevention and Control (ECDC). Surveillance Atlas of Infectious Diseases. Stockholm: ECDC. [Accessed: 29 Feb 2024]. Available from: https://atlas.ecdc.europa.eu/public/index.aspx
  2. European Centre for Disease Prevention and Control (ECDC). Malaria Annual Epidemiological Report for 2021. Stockholm: ECDC; 2023. Available from: https://www.ecdc.europa.eu/en/publications-data/malaria-annual-epidemiological-report-2021
  3. Isaäcson M. Airport malaria: a review. Bull World Health Organ. 1989;67(6):737-43. PMID: 2699278 
  4. Alenou LD, Etang J. Airport malaria in non-endemic areas: new insights into mosquito vectors, case management and major challenges. Microorganisms. 2021;9(10):2160.  https://doi.org/10.3390/microorganisms9102160  PMID: 34683481 
  5. Knobloch K, Yoon U, Vogt PM. Preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement and publication bias. J Craniomaxillofac Surg. 2011;39(2):91-2.  https://doi.org/10.1016/j.jcms.2010.11.001  PMID: 21145753 
  6. Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A. Rayyan-a web and mobile app for systematic reviews. Syst Rev. 2016;5(1):210.  https://doi.org/10.1186/s13643-016-0384-4  PMID: 27919275 
  7. National Institutes of Health (NIH) National Heart Lung and Blood Institute. Quality Assessment Tool for Quality Assessment Tool for Case Series Studies. Bethesda: NIH; 2021. Available from: https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools
  8. Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R, et al. Welcome to the Tidyverse. J Open Source Softw. 2019;4(43):1686.  https://doi.org/10.21105/joss.01686 
  9. Hay SI, Snow RW. The malaria Atlas Project: developing global maps of malaria risk. PLoS Med. 2006;3(12):e473.  https://doi.org/10.1371/journal.pmed.0030473  PMID: 17147467 
  10. Alós JI, Cercenado E, Rodríguez-Créixems M, Erice A, Bouza E. Suspected airport malaria in Spain. Eur J Clin Microbiol. 1985;4(5):509.  https://doi.org/10.1007/BF02014436  PMID: 4065140 
  11. Arends JE, Oosterheert JJ, Kraaij-Dirkzwager MM, Kaan JA, Fanoy EB, Haas PJ, et al. Two cases of Plasmodium falciparum malaria in the Netherlands without recent travel to a malaria-endemic country. Am J Trop Med Hyg. 2013;89(3):527-30.  https://doi.org/10.4269/ajtmh.13-0213  PMID: 23857021 
  12. Baud M, Bauchet E, Poilane I, Levacher S, Pourriat JL. Acute respiratory distress syndrome due to falciparum malaria in a pregnant woman. Intensive Care Med. 1997;23(7):787-9.  https://doi.org/10.1007/s001340050411  PMID: 9290995 
  13. Castelli F, Caligaris S, Matteelli A, Chiodera A, Carosi G, Fausti G. ‘Baggage malaria’ in Italy: cryptic malaria explained? Trans R Soc Trop Med Hyg. 1993;87(4):394.  https://doi.org/10.1016/0035-9203(93)90009-F  PMID: 8249060 
  14. Cheikhrouhou F, Ammar R, Bellili S, Jdidi I, Bahloul M, Ayadi A, et al. Macrophage activation syndrome in a patient affected by Plasmodium falciparum Aeroport malaria. Tunis Med. 2019;97(2):379-82. PMID: 31539098 
  15. Coloigner M, Treguer H, Le Gac A, Le Bihan G. Paludisme contracté en France. [Malaria incurred in France]. Nouv Presse Med. 1978;7(21):1865. PMID: 353710 
  16. Crestia J, Gourmel A, Tredez C, Guiheneuf E, Boyer T. Severe airport malaria complicated by macrophage activation syndrome. Br J Haematol. 2020;191(5):652.  https://doi.org/10.1111/bjh.17064  PMID: 33094847 
  17. Doby JM, Guiguen C. A propos de deux cas "Bretons" de paludisme autochtone, en réalité, premiers cas Français de "paludisme d’aérodrome". [2 Breton cases of autochthonous malaria, in reality the first French cases of "airport malaria"]. Bull Soc Pathol Exot. 1981;74(4):398-405. PMID: 1807855 
  18. Gallien S, Taieb F, Hamane S, De Castro N, Molina JM. Autochthonous falciparum malaria possibly transmitted by luggage-carried vector in Paris, France, February 2013. Euro Surveill. 2013;18(40):20600.  https://doi.org/10.2807/1560-7917.ES2013.18.40.20600  PMID: 24128697 
  19. Hemmer R. Airport malaria in Luxembourg. Euro Surveill. 1999;3(34).
  20. Hennequin C, May F, Treluyer JM, Druilhe P, Valensi F, Pays JF. Les difficultés diagnostiques du paludisme d’aéroport. [Diagnostic challenges of airport malaria]. Hematologie. 1996;2(4):329-33.
  21. Holvoet G, Michielsen P, Vandepitte J. Airport malaria in Belgium. Lancet. 1982;2(8303):881-2.  https://doi.org/10.1016/S0140-6736(82)90849-2  PMID: 6126742 
  22. Larcan A, Laprevote-Heully MC, Voydeville G, Bastos P. Une nouvelle observation de paludisme autochtone avec contamination probable dans un aéroport international de la région parisienne. [A new case of autochthonous malaria with probable contamination in an international airport of the Paris region]. Ann Med Interne (Paris). 1978;129(6-7):411-2. PMID: 356697 
  23. 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.  https://doi.org/10.2807/esm.05.07.00017-en  PMID: 12631852 
  24. Pomares-Estran C, Delaunay P, Mottard A, Cua E, Roger PM, Pradines B, et al. Atypical aetiology of a conjugal fever: autochthonous airport malaria between Paris and French Riviera: a case report. Malar J. 2009;8(1):202.  https://doi.org/10.1186/1475-2875-8-202  PMID: 19698152 
  25. Praetorius F, Altrock G, Blees N, Schuh N, Faulde M. Importierte Anopheles: im Gepäck oder aus dem Flugzeug? Ein Fall von schwerer autochthoner Malaria tropica in Flughafennähe. [Imported Anopheles: in the luggage or from the airplane? A case of severe autochthonous malaria tropica near an airport]. Dtsch Med Wochenschr. 1999;124(34-35):998-1002. PMID: 10488327 
  26. Rabinowitz I, Nasser E, Nassar F, Varkel J. Airport malaria infection in a passenger returning from Germany. Isr Med Assoc J. 2004;6(3):178-9. PMID: 15055277 
  27. Rizzo F, Morandi N, Riccio G, Ghiazza G, Garavelli P. Unusual transmission of falciparum malaria in Italy. Lancet. 1989;1(8637):555-6.  https://doi.org/10.1016/S0140-6736(89)90095-0  PMID: 2564085 
  28. Sabatinelli G, Majori G, D’Ancona F, Romi R. Malaria epidemiological trends in Italy. Eur J Epidemiol. 1994;10(4):399-403.  https://doi.org/10.1007/BF01719663  PMID: 7843343 
  29. Smeaton MJ, Slater PJ, Robson P. Malaria from a "commuter" mosquito. Lancet. 1984;1(8381):845-6.  https://doi.org/10.1016/S0140-6736(84)92288-8  PMID: 6143154 
  30. Thang HD, Elsas RM, Veenstra J. Airport malaria: report of a case and a brief review of the literature. Neth J Med. 2002;60(11):441-3. PMID: 12685493 
  31. Weir WR, Hodges JM, Wright JF, Higgins AF, Corringham RE. Atypical falciparum malaria: case report. Br Med J (Clin Res Ed). 1984;289(6438):178.  https://doi.org/10.1136/bmj.289.6438.178  PMID: 6430402 
  32. Whitfield D, Curtis CF, White GB, Targett GA, Warhurst DC, Bradley DJ. Two cases of falciparum malaria acquired in Britain. Br Med J (Clin Res Ed). 1984;289(6458):1607-9.  https://doi.org/10.1136/bmj.289.6458.1607  PMID: 6439340 
  33. World Health Organization (WHO). Malaria Surveillance. Wkly Epidemiol Rec. 1984;59(45):347.
  34. Wieters I, Eisermann P, Borgans F, Giesbrecht K, Goetsch U, Just-Nübling G, et al. Two cases of airport-associated falciparum malaria in Frankfurt am Main, Germany, October 2019. Euro Surveill. 2019;24(49):1900691.  https://doi.org/10.2807/1560-7917.ES.2019.24.49.1900691  PMID: 31822328 
  35. Aloy A, Laguarda M, Puig A, Capdevila E. Mosquito de los equipajes: una nueva forma de transmisión del paludismo? [Mosquitoes in the luggage: a new form of malaria transmission?]. Med Clin (Barc). 1994;103(6):237-8. PMID: 7967873 
  36. Baixench MT, Suzzoni-Blatger J, Magnaval JF, Lareng MB, Larrouy G. Deux cas inexpliqués de paludisme autochtone a Toulouse, France. [Two cases of inexplicable autochthonous malaria in Toulouse, France]. Med Trop (Mars). 1998;58(1):62-4. PMID: 9718558 
  37. Bentata-Pessayre M, Schnurmann D, Krivitzky A, Callard P, Delzant G. Paludisme autochtone et foie palustre. A propos d’une observation. [Autochthonous malaria and malarian liver. Apropos of 1 case]. Bull Soc Pathol Exot. 1978;71(6):417-23.
  38. Bouvier M, Pittet D, Loutan L, Starobinski M. Paludisme des aéroports: mini-épidémie en Suisse . [Airport malaria: mini-epidemic in Switzerland]. Schweiz Med Wochenschr. 1990;120(34):1217-22. PMID: 2218443 
  39. Delemarre BJM, van der Kaay HJ. Malaria tropica op natuurlijke wijze verkregen in Nederland. [Tropical malaria contracted the natural way in the Netherlands]. Ned Tijdschr Geneeskd. 1979;123(46):1981-2. PMID: 390409 
  40. Delemarre-van de Waal HA, de Waal FC. Een tweede patiënt met malaria tropica op natuurlijke wijze verkregen in Nederland. [A 2d patient with tropical malaria contracted in a natural way in the Netherlands]. Ned Tijdschr Geneeskd. 1981;125(10):375-7. PMID: 7012644 
  41. Gentilini M, Danis M, Dallot JY, Richard-Lenoble D, Felix H. Réapparition du paludisme autochtone? [Reappearance of autochthonous malaria?] Ann Med Interne (Paris). 1978;129(6-7):405-10. PMID: 356696 
  42. Giacomini T, Mouchet J, Mathieu P, Petithory JC. Etude de six cas de paludisme contractés près de Roissy-Charles-de-Gaulle en 1994. Mesures de prévention nécessaires dans les aéroports. [Study of 6 cases of malaria acquired near Roissy-Charles-de-Gaulle in 1994. Necessary prevention measures in airports]. Bull Acad Natl Med. 1995;179(2):335-51, discussion 351-3. PMID: 7614062 
  43. Giacomini T, Toledano D, Baledent F. Gravite du paludisme des aéroports. [The severity of airport malaria]. Bull Soc Pathol Exot. 1988;81(3):345-50.
  44. Marty P, Delaunay P, Ribière C, Terrisse V, Bernard E, Le Fichoux Y, et al. Paludisme autochtone probablement aéroportuaire observé à Nice (France). [Domestic malaria in Nice (France) probably transmitted via the airport]. Presse Med. 2001;30(10):488. PMID: 11307489 
  45. Rosci MA, Paglia MG, De Felici A, Antonucci G, Armignacco O, Cardini A, et al. A case of falciparum malaria acquired in Italy. Trop Geogr Med. 1987;39(1):77-9. PMID: 3299933 
  46. Saliou P.Deux nouveaux cas de paludisme autochtone dans la region Parisienne illustrant deux modes de contamination différents. [Two new autochthonous malaria cases in Paris Region showing two different modes of contamination]. Bull Soc Pathol Exot. 1978;71:324-47.
  47. Van den Ende J, Lynen L, Elsen P, Colebunders R, Demey H, Depraetere K, et al. A cluster of airport malaria in Belgium in 1995. Acta Clin Belg. 1998;53(4):259-63.  https://doi.org/10.1080/17843286.1998.11772033  PMID: 9795446 
  48. Bouza C, Landín L, Díaz Borrego JM, Martín del Yerro JL. Malaria: resurge como enfermedad autóctona en España? [Malaria: is it reappearing as an endemic disease in Spain?] Med Clin (Barc). 1985;84(15):630-1. PMID: 3889521 
  49. Cassaigne R, Bruaire M, Leger N, Ferrand G, Vandamme R, Timbal J. Paludisme autochtone cent ans après Laveran: Le paludisme à Paris. [Autochthonous malaria - one hundred years after Laveran: malaria in Paris]. Cahiers Orston AHIERS.1980;18(2):177-80.
  50. Mantel CF, Klose C, Scheurer S, Vogel R, Wesirow AL, Blenzie U. Plasmodium falciparum malaria acquired in Berlin, Germany. Lancet. 1995;346(8970):320-1.  https://doi.org/10.1016/S0140-6736(95)92212-1  PMID: 7630281 
  51. Marty P, Le Fichoux Y, Izri MA, Mora M, Mora M, Mathieu B, et al. Autochtonous Plasmodium falciparum malaria in southern France. Trans R Soc Trop Med Hyg. 1992;86(5):478.  https://doi.org/10.1016/0035-9203(92)90074-M  PMID: 1475808 
  52. Revel MP, Datry A, Saint Raimond A, Lenoir G, Danis M, Gentilini M. Plasmodium falciparum malaria after three years in a non-endemic area. Trans R Soc Trop Med Hyg. 1988;82(6):832.  https://doi.org/10.1016/0035-9203(88)90008-9  PMID: 3076996 
  53. Van Bortel W, Van den Poel B, Hermans G, Vanden Driessche M, Molzahn H, Deblauwe I, et al. Two fatal autochthonous cases of airport malaria, Belgium, 2020. Euro Surveill. 2022;27(16):2100724.  https://doi.org/10.2807/1560-7917.ES.2022.27.16.2100724  PMID: 35451360 
  54. Brumpt L, Petithory JC, Giacomini T. Actualités du paludisme en France. [News on malaria in France]. Bull Acad Natl Med. 1978;162(5):394-400.
  55. Giacomini T, Mathieu F. Le paludisme des aéroports: un problème de santé publique. [Airport malaria: a public health problem]. Bulletin épidémiologique hebdomadaire. 1996 (29):127-8. French. Available from: https://www.santepubliquefrance.fr/maladies-et-traumatismes/maladies-a-transmission-vectorielle/paludisme/documents/article/le-paludisme-des-aeroports-un-probleme-de-sante-publique
  56. Cuadros J, Calvente MJ, Benito A, Arévalo J, Calero MA, Segura J, et al. Plasmodium ovale malaria acquired in central Spain. Emerg Infect Dis. 2002;8(12):1506-8.  https://doi.org/10.3201/eid0812.020105  PMID: 12498674 
  57. World Health Organization (WHO). Malaria: Five cases of airport malaria. Wkly Epidemiol Rec. 1986;61(30):235-6.
  58. Kessel J, Rosanas-Urgell A, Dingwerth T, Goetsch U, Haller J, Huits R, et al. Investigation of an airport-associated cluster of falciparum malaria in Frankfurt, Germany, 2022. Euro Surveill. 2024;29(5):2300298.  https://doi.org/10.2807/1560-7917.ES.2024.29.5.2300298  PMID: 38304950 
  59. Ashley EA, White NJ. The duration of Plasmodium falciparum infections. Malar J. 2014;13(1):500.  https://doi.org/10.1186/1475-2875-13-500  PMID: 25515943 
  60. Fischer L, Gültekin N, Kaelin MB, Fehr J, Schlagenhauf P. Rising temperature and its impact on receptivity to malaria transmission in Europe: A systematic review. Travel Med Infect Dis. 2020;36:101815.  https://doi.org/10.1016/j.tmaid.2020.101815  PMID: 32629138 
  61. Tatem AJ, Rogers DJ, Hay SI. Global transport networks and infectious disease spread. Adv Parasitol. 2006;62:293-343.  https://doi.org/10.1016/S0065-308X(05)62009-X  PMID: 16647974 
  62. Sun X, Wandelt S, Zheng C, Zhang A. COVID-19 pandemic and air transportation: Successfully navigating the paper hurricane. J Air Transp Manage. 2021;94:102062.  https://doi.org/10.1016/j.jairtraman.2021.102062  PMID: 33875908 
  63. Diouf I, Rodriguez Fonseca B, Caminade C, Thiaw WM, Deme A, Morse AP, et al. Climate variability and malaria over West Africa. Am J Trop Med Hyg. 2020;102(5):1037-47.  https://doi.org/10.4269/ajtmh.19-0062  PMID: 32189612 
  64. Thellier M, Simard F, Musset L, Cot M, Velut G, Kendjo E, et al. Changes in malaria epidemiology in France and worldwide, 2000-2015. Med Mal Infect. 2020;50(2):99-112.  https://doi.org/10.1016/j.medmal.2019.06.002  PMID: 31257063 
  65. United Kingdom (UK) Department of Health. Health Protection (Ships and Aircraft) Regulations: a consultation. London: UK Department of Health; 2013. Available from: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/225162/Health_protection_ships_and_aircrafts_regulations_consultation_document.pdf
  66. European Commission. Commission Implementing Decision (EU) 2018/945 of 22 June 2018 on the communicable diseases and related special health issues to be covered by epidemiological surveillance as well as relevant case definitions. Official Journal of the European Union. 2018;61:170. Available from: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32018D0945&from=EN#page=29
  67. Bastaki H, Carter J, Marston L, Cassell J, Rait G. Time delays in the diagnosis and treatment of malaria in non-endemic countries: A systematic review. Travel Med Infect Dis. 2018;21:21-7.  https://doi.org/10.1016/j.tmaid.2017.12.002  PMID: 29225124 
  68. Balajee SA, Salyer SJ, Greene-Cramer B, Sadek M, Mounts AW. The practice of event-based surveillance: concept and methods. Glob Secur Health Sci Policy. 2021;6(1):1-9.  https://doi.org/10.1080/23779497.2020.1848444 
  69. Pondorfer SG, Jaeger VK, Scholz-Kreisel P, Horn J, Krumkamp R, Kreuels B, et al. Risk estimation for air travel-induced malaria transmission in central Europe - A mathematical modelling study. Travel Med Infect Dis. 2020;36:101564.  https://doi.org/10.1016/j.tmaid.2020.101564  PMID: 32004733 
  70. Pang AM, Gay S, Yadav R, Dolea C, Ponce C, Velayudhan R, et al. The safety and applicability of synthetic pyrethroid insecticides for aircraft disinsection: A systematic review. Travel Med Infect Dis. 2020;33:101570.  https://doi.org/10.1016/j.tmaid.2020.101570  PMID: 32007622 
  71. République Française. Arrêté du 29 novembre 2016 relatif aux zones en provenance desquelles les moyens de transport sont désinsectisés. [Order of 29 November 2016 on the areas from which means of transport are disinsected]. Journal officiel “Lois et Décrets”. 6 Jan 2017. French. Available from: https://www.legifrance.gouv.fr/loda/id/JORFTEXT000033825603/2021-07-31
  72. World Health Organization (WHO). WHO aircraft disinsection methods and procedures, 2nd ed. Geneva: WHO; 2023. Available from: https://www.who.int/publications/i/item/9789240080317
  73. Guillet P, Germain MC, Giacomini T, Chandre F, Akogbeto M, Faye O, et al. Origin and prevention of airport malaria in France. Trop Med Int Health. 1998;3(9):700-5.  https://doi.org/10.1046/j.1365-3156.1998.00296.x  PMID: 9754664 
  74. World Health Organization (WHO). World malaria report 2023. Geneva: WHO; 2023. Available from: https://www.who.int/teams/global-malaria-programme/reports/world-malaria-report-2023
  75. Mohapatra MK, Dash LK, Barih PK, Karua PC. Profile of mixed species (Plasmodium vivax and falciparum) malaria in adults. J Assoc Physicians India. 2012;60:20-4. PMID: 23777020 
  76. Auvergnat JC. Plasmodium falciparum : à propos d'une observation. [Plasmodium falciparum: an observation]. 1979. Rev Med Toulouse. French.
  77. Giacomini T, Goudal H, Boudon P, Rennes C, Dumouchel P, Petithory J. A propos de deux cas de paludisme a Plasmodium falciparum. Responsabilité probable d’anopheles importes par voie aérienne. [Two cases of Plasmodium falciparum malaria. Probable responsibility of Anopheles transported by air]. Bull Soc Pathol Exot. 1977;70(4):375-9.
  78. Razzaq QM. Malaria in a patient with no known risk factors. EMJ-Emirates Medical Journal.2003;21(3):261-2.
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