World Health Organization, 2012. Malaria. International Travel and Health. Geneva, Switzerland: WHO.
Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von Sonnenburg F, Black J, Brown GV, Torresi J; GeoSentinel Surveillance Network, 2006. Illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin Infect Dis 43: 1185–1193.
Schwartz E, Parise M, Kozarsky P, Cetron M, 2003. Delayed onset of malaria—implications for chemoprophylaxis in travelers. N Engl J Med 349: 1510–1516.
D’Ortenzio E, Godineau N, Fontanet A, Houze S, Bouchaud O, Matheron S, Le Bras J, 2008. Prolonged Plasmodium falciparum infection in immigrants, Paris. Emerg Infect Dis 14: 323–326.
Kantele A, Siikamäki H, Hannila‐Handelberg T, Laitinen K, Rombo L, 2012. Plasmodium falciparum malaria in pregnant African immigrants often goes unrecognized. J Travel Med 19: 380–382.
Al Hammadi A, Mitchell M, Abraham GM, Wang JP, 2017. Recrudescence of Plasmodium falciparum in a primigravida after nearly 3 years of latency. Am J Trop Med Hyg 96: 642–644.
Monge-Maillo B, Norman F, Pérez-Molina JA, Díaz-Menéndez M, Rubio JM, López-Vélez R, 2012. Plasmodium falciparum in asymptomatic immigrants from Sub-Saharan Africa, Spain. Emerg Infect Dis 18: 356–357.
Vareil M-O et al. 2011. Unusual transmission of Plasmodium falciparum, Bordeaux, France, 2009. Emerg Infect Dis 17: 248–250.
Isaäcson M, 1989. Airport malaria: a review. Bull World Health Organ 67: 737–743.
Frean J, Brooke B, Thomas J, Blumberg L, 2014. Odyssean malaria outbreaks in Gauteng Province, South Africa, 2007–2013. S Afr Med J 104: 335–338.
Ashley EA, White NJ, 2014. The duration of Plasmodium falciparum infections. Malar J 13: 500.
Moncunill G et al. 2013. High antibody responses against Plasmodium falciparum in immigrants after extended periods of interrupted exposure to malaria. PLoS One 8: e73624.
Bidegain F, Berry A, Alvarez M, Verhille O, Huguet F, Brousset P, Pris J, Marchou B, Magnaval JF, 2005. Acute Plasmodium falciparum malaria following splenectomy for suspected lymphoma in 2 patients. Clin Infect Dis 40: e97–e100.
Howden BP, Vaddadi G, Grayson ML, Manitta J, 2005. Chronic falciparum malaria causing massive splenomegaly 9 years after leaving an endemic area. Med J Aust 182: 186–188.
White NJ, 2017. Malaria parasite clearance. Malar J 16: 88.
Rogerson SJ, Hviid L, Duffy PE, Leke RF, Taylor DW, 2007. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis 7: 105–117.
Flateau C, Le Loup G, Pialoux G, 2011. Consequences of HIV infection on malaria and therapeutic implications: a systematic review. Lancet Infect Dis 11: 541–556.
Weiss GE et al. 2010. The Plasmodium falciparum-specific human memory B cell compartment expands gradually with repeated malaria infections. PLoS Pathog 6: e1000912.
Moir S, Fauci AS, 2017. B-cell responses to HIV infection. Immunol Rev 275: 33–48.
Subramaniam KS, Skinner J, Ivan E, Mutimura E, Kim RS, Feintuch CM, Portugal S, Anastos K, Crompton PD, Daily JP, 2015. HIV malaria co-infection is associated with atypical memory B cell expansion and a reduced antibody response to a broad array of Plasmodium falciparum antigens in Rwandan adults. PLOS One 10: e0124412.
Argy N, Kendjo E, Augé-Courtoi C, Cojean S, Clain J, Houzé P, Thellier M, Hubert V, Deloron P, Houzé S; CNRP study group, 2017. Influence of host factors and parasite biomass on the severity of imported Plasmodium falciparum malaria. PLOS One 12: e0175328.
Vantomme B, Van Acker J, Rogge S, Ommeslag D, Donck J, Callens S, 2016. Plasmodium falciparum malaria occurring four years after leaving an endemic area. Acta Clin Belg 71: 111–113.
Theunissen C, Janssens P, Demulder A, Nouboussié D, Van Esbroeck M, Van Gompel A, Van den Ende J, 2009. Falciparum malaria in patient 9 years after leaving malaria-endemic area. Emerg Infect Dis 15: 115–116.
Arends JE, Oosterheert JJ, Kraaij-Dirkzwager MM, Kaan JA, Fanoy EB, Haas P-J, Scholte E-J, Kortbeek LM, Sankatsing SUC, 2013. Two cases of Plasmodium falciparum malaria in the Netherlands without recent travel to a malaria-endemic country. Am J Trop Med Hyg 89: 527–530.
Gallien S, Taieb F, Hamane S, De Castro N, Molina JM, 2013. Autochthonous falciparum malaria possibly transmitted by luggage-carried vector in Paris, France, February 2013. Euro Surveill 18: 2–3.
Bruneel F, Thellier M, Eloy O, Mazier D, Boulard G, Danis M, Bédos J-P, 2004. Transfusion-transmitted malaria. Intensive Care Med 30: 1851–1852.
European Centre for Disease Prevention and Control, 2017. Multiple Reports of Locally—Acquired Malaria Infections in the EU. Stockolm, Sweden: ECDC.
Aydin-Schmidt B, Xu W, González IJ, Polley SD, Bell D, Shakely D, Msellem MI, Björkman A, Mårtensson A, 2014. Loop mediated isothermal amplification (LAMP) accurately detects malaria DNA from filter paper blood samples of low density parasitaemias. PLoS One 9: e103905.
Carme B, Danis M, Gentilini M, 1978. Longévité de Plasmodium falciparum: à propos de 3 cas d’accès palustres survenus plus de 2 mois après le départ de la zone d’endémie. Med Mal Infect 8: 352–354.
Revel M, Datry A, Saint Raimond A, Lenoir G, Danis M, Gentilini M, 1988. Plasmodium falciparum malaria after three years in a non-endemic area. Trans R Soc Trop Med Hyg 82: 832.
Krajden S, Panisko D, Tobe B, Yang J, Keystone J, 1991. Prolonged infection with Plasmodium falciparum in a semiimmune patient. Trans R Soc Trop Med Hyg 85: 731–732.
Georges P, Houmeau L, Legall MA, Badoual J, Gendrel D, 1992. Late onset Plasmodium falciparum malaria revealed by corticoid therapy. Presse Medicale (Paris, France: 1983) 21: 1434.
Eloy O, Zuily E, Greder-Belan A, Bouchot C, Ghnassia JC, Legros F, 1998. Plasmodium falciparum malaria. 4 years after returning from an endemic zone. Presse Medicale (Paris, France: 1983) 27: 1898.
Omonuwa S, Omonuva S, 2002. Malaria recurrence caused by Plasmodium falciparum. J Am Board Fam Pract 15: 159–160.
Giobbia M, Tonon E, Zanatta A, Cesaris L, Bisoffi Z, Vaglia A, 2005. Late recrudescence of Plasmodium falciparum malaria in a pregnant woman: a case report. Int J Infect Dis 9: 234–235.
Rapp C, Imbert P, Fabre R, Barruet R, Debord T, 2006. Delayed onset Plasmodium falciparum malaria in adults. Med Trop Rev Corps Sante Colon 66: 310.
Szmitko PE, Kohn ML, Simor AE, 2009. Plasmodium falciparum malaria occurring 8 years after leaving an endemic area. Diagn Microbiol Infect Dis 63: 105–107.
Poilane I, Jeantils V, Carbillon L, 2009. Découverte fortuite de paludisme à Plasmodium falciparum au cours de la grossesse: à propos de deux cas. Gynécol Obstét Fertil 37: 824–826.
Cullen KA, Arguin PM, 2013. Malaria surveillance—United States, 2011. MMWR Surveill Summ 62: 1–17.
Berrevoets MA, Sprong T, Meis JF, Dofferhoff ASM. 2013. Plasmodium falciparum malaria recrudescence occurring 2.5 years after leaving an endemic country. Neth J Med 71: 426–428.
Odolini S, Apostoli A, Casari S, Matteelli A, Castelli F, 2014. Recrudescence of Plasmodium falciparum malaria in a primigravid woman with anaemia as the only sign of disease. J Obstet Gynaecol 34: 356.
Martelli G, Girometti N, Vanino E, Bottieau E, Viale P, 2015. Plasmodium falciparum malaria in migrants who transited Libya—where did they contract malaria? Travel Med Infect Dis 13: 499–500.
Dierksen J, Al-Ibraheemi A, Wanger A, Chen L, 2016. Plasmodium falciparum recurrence two years after exposure in endemic country: a case report. Ann Clin Lab Sci 46: 433–434.
Salas-Coronas J, Soriano-Pérez MJ, Pérez-Moyano R, Lozano-Serrano AB, Cabezas-Fernández MT, Porrino-Herrera C, 2017. Symptomatic falciparum malaria after living in a nonendemic area for 10 years: recrudescence or indigenous transmission? Am J Trop Med Hyg 96: 1427–1429.
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Emerging evidence indicates that migrants from Plasmodium falciparum endemic regions are at risk of delayed presentation of P. falciparum malaria. We report three cases of P. falciparum malaria occurring years after arrival in Europe. All patients were originally from Sub-Saharan Africa. Two subjects had controlled human immunodeficiency virus infection and one was a pregnant woman. We performed a literature review of all published cases of delayed presentation of P. falciparum in migrants and identified 32 additional cases. All cases but one originate from sub-Saharan Africa. There was a median time of 36 months between the last visit to a malaria-endemic country and clinical malaria (range: 3 months to 10 years). Pregnancy was the most frequently reported risk factor (11/35 or 31.4%). Parasitemia was ≤ 0.1% in 38% of cases (11/29 reported), and no death was reported. The underlying possible mechanisms for this delayed presentation in migrants from an endemic area probably include the persistence of submicroscopic parasitemia combined with decaying P. falciparum–specific immunity. Suspicion of P. falciparum delayed malaria should remain high in migrants, mainly from sub-Saharan Africa, even without a recent travel history, especially in those presenting risk factors for impaired parasite clearance or distinct immune responses such as pregnancy and HIV infection. In these patients, new prevention and screening strategies should be studied and blood safety policies adapted.
Authors’ addresses: Nicolas Dauby, Deborah Konopnicki, and Charlotte Martin, Infectious Diseases Department, Université Libre de Bruxelles (ULB), CHU Saint-Pierre, Brussels, Belgium, E-mails: nicolas_dauby@stpierre-bru.be, deborah_konopnicki@stpierre-bru.be, and charlotte_martin@stpierre-bru.be. Mariana Figueiredo Ferreira, Internal Medicine Department, CHU Saint-Pierre, Brussels, Belgium, E-mail: mariana_figueiredoferreira@stpierre-bru.be. Vo Thanh Phuong Nguyen and Brigitte Cantinieaux, Hematology Department, LHUB-ULB, Brussels, Belgium, E-mails: phuong.nguyenvothanh@lhub-ulb.be and brigitte.cantinieaux@lhub-ulb.be.
These authors contributed equally to this work.
World Health Organization, 2012. Malaria. International Travel and Health. Geneva, Switzerland: WHO.
Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von Sonnenburg F, Black J, Brown GV, Torresi J; GeoSentinel Surveillance Network, 2006. Illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin Infect Dis 43: 1185–1193.
Schwartz E, Parise M, Kozarsky P, Cetron M, 2003. Delayed onset of malaria—implications for chemoprophylaxis in travelers. N Engl J Med 349: 1510–1516.
D’Ortenzio E, Godineau N, Fontanet A, Houze S, Bouchaud O, Matheron S, Le Bras J, 2008. Prolonged Plasmodium falciparum infection in immigrants, Paris. Emerg Infect Dis 14: 323–326.
Kantele A, Siikamäki H, Hannila‐Handelberg T, Laitinen K, Rombo L, 2012. Plasmodium falciparum malaria in pregnant African immigrants often goes unrecognized. J Travel Med 19: 380–382.
Al Hammadi A, Mitchell M, Abraham GM, Wang JP, 2017. Recrudescence of Plasmodium falciparum in a primigravida after nearly 3 years of latency. Am J Trop Med Hyg 96: 642–644.
Monge-Maillo B, Norman F, Pérez-Molina JA, Díaz-Menéndez M, Rubio JM, López-Vélez R, 2012. Plasmodium falciparum in asymptomatic immigrants from Sub-Saharan Africa, Spain. Emerg Infect Dis 18: 356–357.
Vareil M-O et al. 2011. Unusual transmission of Plasmodium falciparum, Bordeaux, France, 2009. Emerg Infect Dis 17: 248–250.
Isaäcson M, 1989. Airport malaria: a review. Bull World Health Organ 67: 737–743.
Frean J, Brooke B, Thomas J, Blumberg L, 2014. Odyssean malaria outbreaks in Gauteng Province, South Africa, 2007–2013. S Afr Med J 104: 335–338.
Ashley EA, White NJ, 2014. The duration of Plasmodium falciparum infections. Malar J 13: 500.
Moncunill G et al. 2013. High antibody responses against Plasmodium falciparum in immigrants after extended periods of interrupted exposure to malaria. PLoS One 8: e73624.
Bidegain F, Berry A, Alvarez M, Verhille O, Huguet F, Brousset P, Pris J, Marchou B, Magnaval JF, 2005. Acute Plasmodium falciparum malaria following splenectomy for suspected lymphoma in 2 patients. Clin Infect Dis 40: e97–e100.
Howden BP, Vaddadi G, Grayson ML, Manitta J, 2005. Chronic falciparum malaria causing massive splenomegaly 9 years after leaving an endemic area. Med J Aust 182: 186–188.
White NJ, 2017. Malaria parasite clearance. Malar J 16: 88.
Rogerson SJ, Hviid L, Duffy PE, Leke RF, Taylor DW, 2007. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis 7: 105–117.
Flateau C, Le Loup G, Pialoux G, 2011. Consequences of HIV infection on malaria and therapeutic implications: a systematic review. Lancet Infect Dis 11: 541–556.
Weiss GE et al. 2010. The Plasmodium falciparum-specific human memory B cell compartment expands gradually with repeated malaria infections. PLoS Pathog 6: e1000912.
Moir S, Fauci AS, 2017. B-cell responses to HIV infection. Immunol Rev 275: 33–48.
Subramaniam KS, Skinner J, Ivan E, Mutimura E, Kim RS, Feintuch CM, Portugal S, Anastos K, Crompton PD, Daily JP, 2015. HIV malaria co-infection is associated with atypical memory B cell expansion and a reduced antibody response to a broad array of Plasmodium falciparum antigens in Rwandan adults. PLOS One 10: e0124412.
Argy N, Kendjo E, Augé-Courtoi C, Cojean S, Clain J, Houzé P, Thellier M, Hubert V, Deloron P, Houzé S; CNRP study group, 2017. Influence of host factors and parasite biomass on the severity of imported Plasmodium falciparum malaria. PLOS One 12: e0175328.
Vantomme B, Van Acker J, Rogge S, Ommeslag D, Donck J, Callens S, 2016. Plasmodium falciparum malaria occurring four years after leaving an endemic area. Acta Clin Belg 71: 111–113.
Theunissen C, Janssens P, Demulder A, Nouboussié D, Van Esbroeck M, Van Gompel A, Van den Ende J, 2009. Falciparum malaria in patient 9 years after leaving malaria-endemic area. Emerg Infect Dis 15: 115–116.
Arends JE, Oosterheert JJ, Kraaij-Dirkzwager MM, Kaan JA, Fanoy EB, Haas P-J, Scholte E-J, Kortbeek LM, Sankatsing SUC, 2013. Two cases of Plasmodium falciparum malaria in the Netherlands without recent travel to a malaria-endemic country. Am J Trop Med Hyg 89: 527–530.
Gallien S, Taieb F, Hamane S, De Castro N, Molina JM, 2013. Autochthonous falciparum malaria possibly transmitted by luggage-carried vector in Paris, France, February 2013. Euro Surveill 18: 2–3.
Bruneel F, Thellier M, Eloy O, Mazier D, Boulard G, Danis M, Bédos J-P, 2004. Transfusion-transmitted malaria. Intensive Care Med 30: 1851–1852.
European Centre for Disease Prevention and Control, 2017. Multiple Reports of Locally—Acquired Malaria Infections in the EU. Stockolm, Sweden: ECDC.
Aydin-Schmidt B, Xu W, González IJ, Polley SD, Bell D, Shakely D, Msellem MI, Björkman A, Mårtensson A, 2014. Loop mediated isothermal amplification (LAMP) accurately detects malaria DNA from filter paper blood samples of low density parasitaemias. PLoS One 9: e103905.
Carme B, Danis M, Gentilini M, 1978. Longévité de Plasmodium falciparum: à propos de 3 cas d’accès palustres survenus plus de 2 mois après le départ de la zone d’endémie. Med Mal Infect 8: 352–354.
Revel M, Datry A, Saint Raimond A, Lenoir G, Danis M, Gentilini M, 1988. Plasmodium falciparum malaria after three years in a non-endemic area. Trans R Soc Trop Med Hyg 82: 832.
Krajden S, Panisko D, Tobe B, Yang J, Keystone J, 1991. Prolonged infection with Plasmodium falciparum in a semiimmune patient. Trans R Soc Trop Med Hyg 85: 731–732.
Georges P, Houmeau L, Legall MA, Badoual J, Gendrel D, 1992. Late onset Plasmodium falciparum malaria revealed by corticoid therapy. Presse Medicale (Paris, France: 1983) 21: 1434.
Eloy O, Zuily E, Greder-Belan A, Bouchot C, Ghnassia JC, Legros F, 1998. Plasmodium falciparum malaria. 4 years after returning from an endemic zone. Presse Medicale (Paris, France: 1983) 27: 1898.
Omonuwa S, Omonuva S, 2002. Malaria recurrence caused by Plasmodium falciparum. J Am Board Fam Pract 15: 159–160.
Giobbia M, Tonon E, Zanatta A, Cesaris L, Bisoffi Z, Vaglia A, 2005. Late recrudescence of Plasmodium falciparum malaria in a pregnant woman: a case report. Int J Infect Dis 9: 234–235.
Rapp C, Imbert P, Fabre R, Barruet R, Debord T, 2006. Delayed onset Plasmodium falciparum malaria in adults. Med Trop Rev Corps Sante Colon 66: 310.
Szmitko PE, Kohn ML, Simor AE, 2009. Plasmodium falciparum malaria occurring 8 years after leaving an endemic area. Diagn Microbiol Infect Dis 63: 105–107.
Poilane I, Jeantils V, Carbillon L, 2009. Découverte fortuite de paludisme à Plasmodium falciparum au cours de la grossesse: à propos de deux cas. Gynécol Obstét Fertil 37: 824–826.
Cullen KA, Arguin PM, 2013. Malaria surveillance—United States, 2011. MMWR Surveill Summ 62: 1–17.
Berrevoets MA, Sprong T, Meis JF, Dofferhoff ASM. 2013. Plasmodium falciparum malaria recrudescence occurring 2.5 years after leaving an endemic country. Neth J Med 71: 426–428.
Odolini S, Apostoli A, Casari S, Matteelli A, Castelli F, 2014. Recrudescence of Plasmodium falciparum malaria in a primigravid woman with anaemia as the only sign of disease. J Obstet Gynaecol 34: 356.
Martelli G, Girometti N, Vanino E, Bottieau E, Viale P, 2015. Plasmodium falciparum malaria in migrants who transited Libya—where did they contract malaria? Travel Med Infect Dis 13: 499–500.
Dierksen J, Al-Ibraheemi A, Wanger A, Chen L, 2016. Plasmodium falciparum recurrence two years after exposure in endemic country: a case report. Ann Clin Lab Sci 46: 433–434.
Salas-Coronas J, Soriano-Pérez MJ, Pérez-Moyano R, Lozano-Serrano AB, Cabezas-Fernández MT, Porrino-Herrera C, 2017. Symptomatic falciparum malaria after living in a nonendemic area for 10 years: recrudescence or indigenous transmission? Am J Trop Med Hyg 96: 1427–1429.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 936 | 735 | 155 |
Full Text Views | 867 | 20 | 7 |
PDF Downloads | 355 | 20 | 3 |