Skip to main content
Top
Published in: Malaria Journal 1/2010

Open Access 01-12-2010 | Research

Declining incidence of imported malaria in the Netherlands, 2000-2007

Authors: Gini GC van Rijckevorsel, Gerard JB Sonder, Ronald B Geskus, Jose CFM Wetsteyn, Robert J Ligthelm, Leo G Visser, Monique Keuter, Perry JJ van Genderen, Anneke van den Hoek

Published in: Malaria Journal | Issue 1/2010

Login to get access

Abstract

Background

To describe the epidemiology and trends of imported malaria in the Netherlands from 2000 through 2007.

Methods

Based on national surveillance data regarding all reported infections of imported malaria, diagnosed 2000 through 2007, incidence and trends of imported malaria in the Netherlands were estimated. Travellers statistics were used to estimate incidence, and data on malaria chemoprophylaxis prescriptions were used to estimate the number of unprotected travellers.

Results

Importation of malaria to the Netherlands is declining even as more travellers visit malaria-endemic countries. On average, 82% were acquired in sub-Saharan Africa, and 75% were caused by Plasmodium falciparum. The overall incidence in imported falciparum malaria fell from 21.5 to 6.6/10,000 of unprotected travellers. The percentage of unprotected travellers rose from 47% to 52% of all travellers. The incidence of imported falciparum infections is greatest from Middle and West Africa, and decreased from 121.3 to 36.5/10,000 travellers. The import of malaria from this region by immigrants visiting friends and relatives (VFR) decreased from 138 infections in 2000, to 69 infections in 2007.

Conclusion

The annual number of imported malaria shows a continuing declining trend, even with an increasing number of travellers visiting malaria endemic countries. VFR import less malaria than previously, and contribute largely to the declining incidence seen. The decline is not readily explained by increased use of chemoprophylaxis and may reflect a reduced risk of infection due to decreasing local malaria transmission as observed in some malaria endemic areas. Nevertheless, the increasing number of unprotected travellers remains worrisome.
Appendix
Available only for authorised users
Literature
1.
go back to reference Kain KC, Keystone JS: Malaria in travelers. Epidemiology, disease, and prevention. Infect Dis Clin North Am. 1998, 12: 267-284. 10.1016/S0891-5520(05)70005-2.CrossRefPubMed Kain KC, Keystone JS: Malaria in travelers. Epidemiology, disease, and prevention. Infect Dis Clin North Am. 1998, 12: 267-284. 10.1016/S0891-5520(05)70005-2.CrossRefPubMed
3.
go back to reference Ladhani S, Aibara RJ, Riordan FA, Shingadia D: Imported malaria in children: a review of clinical studies. Lancet Infect Dis. 2007, 7: 349-357. 10.1016/S1473-3099(07)70110-X.CrossRefPubMed Ladhani S, Aibara RJ, Riordan FA, Shingadia D: Imported malaria in children: a review of clinical studies. Lancet Infect Dis. 2007, 7: 349-357. 10.1016/S1473-3099(07)70110-X.CrossRefPubMed
4.
go back to reference Smith AD, Bradley DJ, Smith V, Blaze M, Behrens RH, Chiodini PL, Whitty CJ: Imported malaria and high risk groups: observational study using UK surveillance data 1987-2006. BMJ. 2008, 337: a120-10.1136/bmj.a120.PubMedCentralCrossRefPubMed Smith AD, Bradley DJ, Smith V, Blaze M, Behrens RH, Chiodini PL, Whitty CJ: Imported malaria and high risk groups: observational study using UK surveillance data 1987-2006. BMJ. 2008, 337: a120-10.1136/bmj.a120.PubMedCentralCrossRefPubMed
5.
go back to reference Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von SF, Black J, Brown GV, Torresi J: Illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin Infect Dis. 2006, 43: 1185-1193. 10.1086/507893.CrossRefPubMed Leder K, Tong S, Weld L, Kain KC, Wilder-Smith A, von SF, Black J, Brown GV, Torresi J: Illness in travelers visiting friends and relatives: a review of the GeoSentinel Surveillance Network. Clin Infect Dis. 2006, 43: 1185-1193. 10.1086/507893.CrossRefPubMed
6.
go back to reference Schlagenhauf P, Steffen R, Loutan L: Migrants as a major risk group for imported malaria in European countries. J Travel Med. 2003, 10: 106-107. 10.2310/7060.2003.31764.CrossRefPubMed Schlagenhauf P, Steffen R, Loutan L: Migrants as a major risk group for imported malaria in European countries. J Travel Med. 2003, 10: 106-107. 10.2310/7060.2003.31764.CrossRefPubMed
7.
go back to reference Muentener P, Schlagenhauf P, Steffen R: Imported malaria (1985-95): trends and perspectives. Bull World Health Organ. 1999, 77: 560-566.PubMedCentralPubMed Muentener P, Schlagenhauf P, Steffen R: Imported malaria (1985-95): trends and perspectives. Bull World Health Organ. 1999, 77: 560-566.PubMedCentralPubMed
8.
go back to reference Sabatinelli G, Ejov M, Joergensen P: Malaria in the WHO European Region (1971-1999). Euro Surveill. 2001, 6: 61-65.PubMed Sabatinelli G, Ejov M, Joergensen P: Malaria in the WHO European Region (1971-1999). Euro Surveill. 2001, 6: 61-65.PubMed
9.
go back to reference Toovey S, Jamieson A: Rolling back malaria: how well is Europe doing?. Travel Med Infect Dis. 2003, 1: 167-175. 10.1016/j.tmaid.2003.09.004.CrossRefPubMed Toovey S, Jamieson A: Rolling back malaria: how well is Europe doing?. Travel Med Infect Dis. 2003, 1: 167-175. 10.1016/j.tmaid.2003.09.004.CrossRefPubMed
10.
go back to reference van Hest NA, Smit F, Verhave JP: Underreporting of malaria incidence in The Netherlands: results from a capture-recapture study. Epidemiol Infect. 2002, 129: 371-377. 10.1017/S0950268802007306.PubMedCentralCrossRefPubMed van Hest NA, Smit F, Verhave JP: Underreporting of malaria incidence in The Netherlands: results from a capture-recapture study. Epidemiol Infect. 2002, 129: 371-377. 10.1017/S0950268802007306.PubMedCentralCrossRefPubMed
11.
go back to reference Malaria Working Group of the National Coordination Centre for Travelers' Health Advice (LCR): Malariaprofylaxe Bulletin. 2009 Malaria Working Group of the National Coordination Centre for Travelers' Health Advice (LCR): Malariaprofylaxe Bulletin. 2009
14.
go back to reference Durrleman S, Simon R: Flexible regression models with cubic splines. Stat Med. 1989, 8: 551-561. 10.1002/sim.4780080504.CrossRefPubMed Durrleman S, Simon R: Flexible regression models with cubic splines. Stat Med. 1989, 8: 551-561. 10.1002/sim.4780080504.CrossRefPubMed
15.
go back to reference Wetsteyn JC, de Geus GA: Falciparum malaria, imported into The Netherlands, 1979-1988. I. Epidemiological aspects. Trop Geogr Med. 1995, 47: 53-60.PubMed Wetsteyn JC, de Geus GA: Falciparum malaria, imported into The Netherlands, 1979-1988. I. Epidemiological aspects. Trop Geogr Med. 1995, 47: 53-60.PubMed
16.
go back to reference Sonder GJB, Van der Plas SM: Malaria Notifications in 2005; Evaluation of LCR-guidelines for malaria prophylaxis. Infectieziekten Bulletin. 2006, 07: 249-252. Sonder GJB, Van der Plas SM: Malaria Notifications in 2005; Evaluation of LCR-guidelines for malaria prophylaxis. Infectieziekten Bulletin. 2006, 07: 249-252.
17.
go back to reference Mali S, Steele S, Slutsker L, Arguin PM: Malaria surveillance--United States, 2007. MMWR Surveill Summ. 2009, 58: 1-16. Mali S, Steele S, Slutsker L, Arguin PM: Malaria surveillance--United States, 2007. MMWR Surveill Summ. 2009, 58: 1-16.
18.
go back to reference van der Eerden LJM, Bosman A, Visser LG: Malaria reported in the Netherlands in 2002; less malaria. Infectieziekten Bulletin. 2003, 12: 419-423. van der Eerden LJM, Bosman A, Visser LG: Malaria reported in the Netherlands in 2002; less malaria. Infectieziekten Bulletin. 2003, 12: 419-423.
19.
go back to reference Williams CJ, Jones J, Chiodini P: High case-fatality from falciparum malaria in UK travellers returning from The Gambia: a case series. Travel Med Infect Dis. 2007, 5: 295-300. 10.1016/j.tmaid.2007.05.001.CrossRefPubMed Williams CJ, Jones J, Chiodini P: High case-fatality from falciparum malaria in UK travellers returning from The Gambia: a case series. Travel Med Infect Dis. 2007, 5: 295-300. 10.1016/j.tmaid.2007.05.001.CrossRefPubMed
20.
go back to reference Hamer DH, Connor BA: Travel health knowledge, attitudes and practices among United States travelers. J Travel Med. 2004, 11: 23-26. 10.2310/7060.2004.13577.CrossRefPubMed Hamer DH, Connor BA: Travel health knowledge, attitudes and practices among United States travelers. J Travel Med. 2004, 11: 23-26. 10.2310/7060.2004.13577.CrossRefPubMed
21.
go back to reference van Herck K, van Damme P, Castelli F, Zuckerman J, Nothdurft H, Dahlgren AL, Gisler S, Steffen R, Gargalianos P, Lopez-Velez R, Overbosch D, Caumes E, Walker E: Knowledge, attitudes and practices in travel-related infectious diseases: the European airport survey. J Travel Med. 2004, 11: 3-8. 10.2310/7060.2004.13609.CrossRefPubMed van Herck K, van Damme P, Castelli F, Zuckerman J, Nothdurft H, Dahlgren AL, Gisler S, Steffen R, Gargalianos P, Lopez-Velez R, Overbosch D, Caumes E, Walker E: Knowledge, attitudes and practices in travel-related infectious diseases: the European airport survey. J Travel Med. 2004, 11: 3-8. 10.2310/7060.2004.13609.CrossRefPubMed
22.
go back to reference Baas MC, Wetsteyn JC, van GT: Patterns of imported malaria at the academic medical center, Amsterdam, the Netherlands. J Travel Med. 2006, 13: 2-7. 10.1111/j.1708-8305.2006.00003.x.CrossRefPubMed Baas MC, Wetsteyn JC, van GT: Patterns of imported malaria at the academic medical center, Amsterdam, the Netherlands. J Travel Med. 2006, 13: 2-7. 10.1111/j.1708-8305.2006.00003.x.CrossRefPubMed
23.
go back to reference Zuckerman JN, Batty AJ, Jones ME: Effectiveness of malaria chemoprophylaxis against Plasmodium falciparum infection in UK travellers: retrospective observational data. Travel Med Infect Dis. 2009, 7: 329-36. 10.1016/j.tmaid.2009.10.002.CrossRefPubMed Zuckerman JN, Batty AJ, Jones ME: Effectiveness of malaria chemoprophylaxis against Plasmodium falciparum infection in UK travellers: retrospective observational data. Travel Med Infect Dis. 2009, 7: 329-36. 10.1016/j.tmaid.2009.10.002.CrossRefPubMed
24.
go back to reference Camus D, Djossou F, Schilthuis HJ, Hogh B, Dutoit E, Malvy D, Roskell NS, Hedgley C, De Boever EH, Miller GB: Atovaquone-proguanil versus chloroquine-proguanil for malaria prophylaxis in nonimmune pediatric travelers: results of an international, randomized, open-label study. Clin Infect Dis. 2004, 38: 1716-1723. 10.1086/421086.CrossRefPubMed Camus D, Djossou F, Schilthuis HJ, Hogh B, Dutoit E, Malvy D, Roskell NS, Hedgley C, De Boever EH, Miller GB: Atovaquone-proguanil versus chloroquine-proguanil for malaria prophylaxis in nonimmune pediatric travelers: results of an international, randomized, open-label study. Clin Infect Dis. 2004, 38: 1716-1723. 10.1086/421086.CrossRefPubMed
25.
go back to reference Hogh B, Clarke PD, Camus D, Nothdurft HD, Overbosch D, Gunther M, Joubert I, Kain KC, Shaw D, Roskell NS, Chulay JD: Atovaquone-proguanil versus chloroquine-proguanil for malaria prophylaxis in non-immune travellers: a randomised, double-blind study. Malarone International Study Team. Lancet. 2000, 356: 1888-1894. 10.1016/S0140-6736(00)03260-8.CrossRefPubMed Hogh B, Clarke PD, Camus D, Nothdurft HD, Overbosch D, Gunther M, Joubert I, Kain KC, Shaw D, Roskell NS, Chulay JD: Atovaquone-proguanil versus chloroquine-proguanil for malaria prophylaxis in non-immune travellers: a randomised, double-blind study. Malarone International Study Team. Lancet. 2000, 356: 1888-1894. 10.1016/S0140-6736(00)03260-8.CrossRefPubMed
26.
go back to reference Overbosch D, Schilthuis H, Bienzle U, Behrens RH, Kain KC, Clarke PD, Toovey S, Knobloch J, Nothdurft HD, Shaw D, Roskell NS, Chulay JD: Atovaquone-proguanil versus mefloquine for malaria prophylaxis in nonimmune travelers: results from a randomized, double-blind study. Clin Infect Dis. 2001, 33: 1015-1021. 10.1086/322694.CrossRefPubMed Overbosch D, Schilthuis H, Bienzle U, Behrens RH, Kain KC, Clarke PD, Toovey S, Knobloch J, Nothdurft HD, Shaw D, Roskell NS, Chulay JD: Atovaquone-proguanil versus mefloquine for malaria prophylaxis in nonimmune travelers: results from a randomized, double-blind study. Clin Infect Dis. 2001, 33: 1015-1021. 10.1086/322694.CrossRefPubMed
27.
go back to reference Abraham C, Clift S, Grabowski P: Cognitive predictors of adherence to malaria prophylaxis regimens on return from a malarious region: a prospective study. Soc Sci Med. 1999, 48: 1641-1654. 10.1016/S0277-9536(98)00455-9.CrossRefPubMed Abraham C, Clift S, Grabowski P: Cognitive predictors of adherence to malaria prophylaxis regimens on return from a malarious region: a prospective study. Soc Sci Med. 1999, 48: 1641-1654. 10.1016/S0277-9536(98)00455-9.CrossRefPubMed
28.
go back to reference Laverone E, Boccalini S, Bechini A, Belli S, Santini MG, Baretti S, Circelli G, Taras F, Banchi S, Bonanni P: Travelers' compliance to prophylactic measures and behavior during stay abroad: results of a retrospective study of subjects returning to a travel medicine center in Italy. J Travel Med. 2006, 13: 338-344. 10.1111/j.1708-8305.2006.00068.x.CrossRefPubMed Laverone E, Boccalini S, Bechini A, Belli S, Santini MG, Baretti S, Circelli G, Taras F, Banchi S, Bonanni P: Travelers' compliance to prophylactic measures and behavior during stay abroad: results of a retrospective study of subjects returning to a travel medicine center in Italy. J Travel Med. 2006, 13: 338-344. 10.1111/j.1708-8305.2006.00068.x.CrossRefPubMed
29.
go back to reference Valve K, Ruotsalainen E, Kärki T, Pekkanen E, Siikamaki H: Cluster of imported malaria from Gambia in Finland--travellers do not listen to given advice. Euro Surveill. 2008, 13 (51): pii: 19068- Valve K, Ruotsalainen E, Kärki T, Pekkanen E, Siikamaki H: Cluster of imported malaria from Gambia in Finland--travellers do not listen to given advice. Euro Surveill. 2008, 13 (51): pii: 19068-
30.
go back to reference Behrens RH, Carroll B, Smith V, Alexander N: Declining incidence of malaria imported into the UK from West Africa. Malar J. 2008, 7: 235-10.1186/1475-2875-7-235.PubMedCentralCrossRefPubMed Behrens RH, Carroll B, Smith V, Alexander N: Declining incidence of malaria imported into the UK from West Africa. Malar J. 2008, 7: 235-10.1186/1475-2875-7-235.PubMedCentralCrossRefPubMed
31.
go back to reference Robert V, Macintyre K, Keating J, Trape JF, Duchemin JB, Warren M, Beier JC: Malaria transmission in urban sub-Saharan Africa. Am J Trop Med Hyg. 2003, 68: 169-176.PubMed Robert V, Macintyre K, Keating J, Trape JF, Duchemin JB, Warren M, Beier JC: Malaria transmission in urban sub-Saharan Africa. Am J Trop Med Hyg. 2003, 68: 169-176.PubMed
32.
go back to reference Ceesay SJ, Casals-Pascual C, Erskine J, Anya SE, Duah NO, Fulford AJ, Sesay SS, Abubakar I, Dunyo S, Sey O, Palmer A, Fofana M, Corrah T, Bojang KA, Whittle HC, Greenwood BM, Conway DJ: Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet. 2008, 372: 1545-1554. 10.1016/S0140-6736(08)61654-2.PubMedCentralCrossRefPubMed Ceesay SJ, Casals-Pascual C, Erskine J, Anya SE, Duah NO, Fulford AJ, Sesay SS, Abubakar I, Dunyo S, Sey O, Palmer A, Fofana M, Corrah T, Bojang KA, Whittle HC, Greenwood BM, Conway DJ: Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet. 2008, 372: 1545-1554. 10.1016/S0140-6736(08)61654-2.PubMedCentralCrossRefPubMed
33.
go back to reference Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, Kabaria CW, Manh BH, Elyazar IR, Brooker S, Smith DL, Moyeed RA, Snow RW: A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med. 2009, 6: e1000048-PubMedCentralCrossRefPubMed Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, Kabaria CW, Manh BH, Elyazar IR, Brooker S, Smith DL, Moyeed RA, Snow RW: A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med. 2009, 6: e1000048-PubMedCentralCrossRefPubMed
34.
go back to reference Schilthuis HJ, Goossens I, Ligthelm RJ, de Vlas SJ, Varkevisser C, Richardus JH: Factors determining use of pre-travel preventive health services by West African immigrants in The Netherlands. Trop Med Int Health. 2007, 12: 990-998. 10.1111/j.1365-3156.2007.01856.x.CrossRefPubMed Schilthuis HJ, Goossens I, Ligthelm RJ, de Vlas SJ, Varkevisser C, Richardus JH: Factors determining use of pre-travel preventive health services by West African immigrants in The Netherlands. Trop Med Int Health. 2007, 12: 990-998. 10.1111/j.1365-3156.2007.01856.x.CrossRefPubMed
35.
go back to reference Jelinek T, Schade LC, Siikamaki H, Myrvang B, Chiodini P, Gascon J, Visser L, Kapaun A, Just-Nubling G: European cluster of imported falciparum malaria from Gambia. Euro Surveill. 2008, 13: 1907- Jelinek T, Schade LC, Siikamaki H, Myrvang B, Chiodini P, Gascon J, Visser L, Kapaun A, Just-Nubling G: European cluster of imported falciparum malaria from Gambia. Euro Surveill. 2008, 13: 1907-
36.
go back to reference Behrens RH, Carroll B, Beran J, Bouchaud O, Hellgren U, Hatz C, Jelinek T, Legros F, Muhlberger N, Myrvang B, Siikamaki H, Visser L: The low and declining risk of malaria in travellers to Latin America: is there still an indication for chemoprophylaxis?. Malar J. 2007, 6 (114): 114-10.1186/1475-2875-6-114.PubMedCentralCrossRefPubMed Behrens RH, Carroll B, Beran J, Bouchaud O, Hellgren U, Hatz C, Jelinek T, Legros F, Muhlberger N, Myrvang B, Siikamaki H, Visser L: The low and declining risk of malaria in travellers to Latin America: is there still an indication for chemoprophylaxis?. Malar J. 2007, 6 (114): 114-10.1186/1475-2875-6-114.PubMedCentralCrossRefPubMed
37.
go back to reference Behrens RH, Bisoffi Z, Bjorkman A, Gascon J, Hatz C, Jelinek T, Legros F, Muhlberger N, Voltersvik P: Malaria prophylaxis policy for travellers from Europe to the Indian Subcontinent. Malar J. 2006, 5: 7-10.1186/1475-2875-5-7.PubMedCentralCrossRefPubMed Behrens RH, Bisoffi Z, Bjorkman A, Gascon J, Hatz C, Jelinek T, Legros F, Muhlberger N, Voltersvik P: Malaria prophylaxis policy for travellers from Europe to the Indian Subcontinent. Malar J. 2006, 5: 7-10.1186/1475-2875-5-7.PubMedCentralCrossRefPubMed
Metadata
Title
Declining incidence of imported malaria in the Netherlands, 2000-2007
Authors
Gini GC van Rijckevorsel
Gerard JB Sonder
Ronald B Geskus
Jose CFM Wetsteyn
Robert J Ligthelm
Leo G Visser
Monique Keuter
Perry JJ van Genderen
Anneke van den Hoek
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2010
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-9-300

Other articles of this Issue 1/2010

Malaria Journal 1/2010 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.