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Published in: Malaria Journal 1/2013

Open Access 01-12-2013 | Research

Global malaria connectivity through air travel

Authors: Zhuojie Huang, Andrew J Tatem

Published in: Malaria Journal | Issue 1/2013

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Abstract

Background

Air travel has expanded at an unprecedented rate and continues to do so. Its effects have been seen on malaria in rates of imported cases, local outbreaks in non-endemic areas and the global spread of drug resistance. With elimination and global eradication back on the agenda, changing levels and compositions of imported malaria in malaria-free countries, and the threat of artemisinin resistance spreading from Southeast Asia, there is a need to better understand how the modern flow of air passengers connects each Plasmodium falciparum- and Plasmodium vivax-endemic region to the rest of the world.

Methods

Recently constructed global P. falciparum and P.vivax malaria risk maps, along with data on flight schedules and modelled passenger flows across the air network, were combined to describe and quantify global malaria connectivity through air travel. Network analysis approaches were then utilized to describe and quantify the patterns that exist in passenger flows weighted by malaria prevalence. Finally, the connectivity within and to the Southeast Asia region where the threat of imported artemisinin resistance arising is highest, was examined to highlight risk routes for its spread.

Results

The analyses demonstrate the substantial connectivity that now exists between and from malaria-endemic regions through air travel. While the air network provides connections to previously isolated malarious regions, it is clear that great variations exist, with significant regional communities of airports connected by higher rates of flow standing out. The structures of these communities are often not geographically coherent, with historical, economic and cultural ties evident, and variations between P. falciparum and P. vivax clear. Moreover, results highlight how well connected the malaria-endemic areas of Africa are now to Southeast Asia, illustrating the many possible routes that artemisinin-resistant strains could take.

Discussion

The continuing growth in air travel is playing an important role in the global epidemiology of malaria, with the endemic world becoming increasingly connected to both malaria-free areas and other endemic regions. The research presented here provides an initial effort to quantify and analyse the connectivity that exists across the malaria-endemic world through air travel, and provide a basic assessment of the risks it results in for movement of infections.
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Literature
2.
go back to reference IATA: IATA 2012 Annual Review. 2012, Beijing: IATA IATA: IATA 2012 Annual Review. 2012, Beijing: IATA
3.
go back to reference Tatem AJ, Huang Z, Das A, Qi Q, Roth J, Qiu Y: Air travel and vector-borne disease movement. Parasitology. 2012, 139: 1816-1830. 10.1017/S0031182012000352.CrossRefPubMed Tatem AJ, Huang Z, Das A, Qi Q, Roth J, Qiu Y: Air travel and vector-borne disease movement. Parasitology. 2012, 139: 1816-1830. 10.1017/S0031182012000352.CrossRefPubMed
4.
go back to reference World Health Organization: The world health report 2007 - A safer future: global public health security in the 21st century. 2007, Geneva: WHO Press World Health Organization: The world health report 2007 - A safer future: global public health security in the 21st century. 2007, Geneva: WHO Press
5.
go back to reference Khan K, McNabb SJ, Memish ZA, Eckhardt R, Hu W, Kossowsky D, Sears J, Arino J, Johansson A, Barbeschi M, McCloskey B, Henry B, Cetron M, Brownstein JS: Infectious disease surveillance and modelling across geographic frontiers and scientific specialties. Lancet Infect Dis. 2012, 12: 222-230. 10.1016/S1473-3099(11)70313-9.CrossRefPubMed Khan K, McNabb SJ, Memish ZA, Eckhardt R, Hu W, Kossowsky D, Sears J, Arino J, Johansson A, Barbeschi M, McCloskey B, Henry B, Cetron M, Brownstein JS: Infectious disease surveillance and modelling across geographic frontiers and scientific specialties. Lancet Infect Dis. 2012, 12: 222-230. 10.1016/S1473-3099(11)70313-9.CrossRefPubMed
6.
go back to reference Huang Z, Das A, Qiu Y, Tatem AJ: Web-based GIS: the vector-borne disease airline importation risk (VBD-AIR) tool. Int J Health Geogr. 2012, 11: 33-10.1186/1476-072X-11-33.PubMedCentralCrossRefPubMed Huang Z, Das A, Qiu Y, Tatem AJ: Web-based GIS: the vector-borne disease airline importation risk (VBD-AIR) tool. Int J Health Geogr. 2012, 11: 33-10.1186/1476-072X-11-33.PubMedCentralCrossRefPubMed
7.
go back to reference Odolini S, Parola P, Gkrania-Klotsas E, Caumes E, Schlagenhauf P, López-Vélez R, Burchard G-D, Santos-O’Connor F, Weld L, von Sonnenburg F, Field V, de Vries P, Jensenius M, Loutan L, Castelli F: Travel-related imported infections in Europe, EuroTravNet 2009. Clin Microbiol Infect. 2012, 18: 468-474. 10.1111/j.1469-0691.2011.03596.x.CrossRefPubMed Odolini S, Parola P, Gkrania-Klotsas E, Caumes E, Schlagenhauf P, López-Vélez R, Burchard G-D, Santos-O’Connor F, Weld L, von Sonnenburg F, Field V, de Vries P, Jensenius M, Loutan L, Castelli F: Travel-related imported infections in Europe, EuroTravNet 2009. Clin Microbiol Infect. 2012, 18: 468-474. 10.1111/j.1469-0691.2011.03596.x.CrossRefPubMed
8.
go back to reference Checkley AM, Smith A, Smith V, Blaze M, Bradley D, Chiodini PL, Whitty CJM: Risk factors for mortality from imported falciparum malaria in the United Kingdom over 20 years: an observational study. BMJ. 2012, 344: e2116-e2116. 10.1136/bmj.e2116.PubMedCentralCrossRefPubMed Checkley AM, Smith A, Smith V, Blaze M, Bradley D, Chiodini PL, Whitty CJM: Risk factors for mortality from imported falciparum malaria in the United Kingdom over 20 years: an observational study. BMJ. 2012, 344: e2116-e2116. 10.1136/bmj.e2116.PubMedCentralCrossRefPubMed
9.
go back to reference Askling HH, Bruneel F, Buchard G, Castelli F, Chiodini PL, Grobusch MP, Lopez-Vélez R, Paul M, Petersen E, Popescu C, Ramharter M, Schlagenhauf P: Management of imported malaria in Europe. Malar J. 2012, 11: 328-10.1186/1475-2875-11-328.PubMedCentralCrossRefPubMed Askling HH, Bruneel F, Buchard G, Castelli F, Chiodini PL, Grobusch MP, Lopez-Vélez R, Paul M, Petersen E, Popescu C, Ramharter M, Schlagenhauf P: Management of imported malaria in Europe. Malar J. 2012, 11: 328-10.1186/1475-2875-11-328.PubMedCentralCrossRefPubMed
10.
go back to reference Abanyie FA, Arguin PM, Gutman J: State of malaria diagnostic testing at clinical laboratories in the United States, 2010: a nationwide survey. Malar J. 2011, 10: 340-10.1186/1475-2875-10-340.PubMedCentralCrossRefPubMed Abanyie FA, Arguin PM, Gutman J: State of malaria diagnostic testing at clinical laboratories in the United States, 2010: a nationwide survey. Malar J. 2011, 10: 340-10.1186/1475-2875-10-340.PubMedCentralCrossRefPubMed
11.
go back to reference Kain K, Harrington M, Tennyson S, Keystone J: Imported malaria: prospective analysis of problems in diagnosis and management. Clin Infect Dis. 1998, 27: 142-149. 10.1086/514616.CrossRefPubMed Kain K, Harrington M, Tennyson S, Keystone J: Imported malaria: prospective analysis of problems in diagnosis and management. Clin Infect Dis. 1998, 27: 142-149. 10.1086/514616.CrossRefPubMed
12.
go back to reference Nilles EJ, Arguin PM: Imported malaria: an update. Am J Emerg Med. 2012, 30: 972-980. 10.1016/j.ajem.2011.06.016.CrossRefPubMed Nilles EJ, Arguin PM: Imported malaria: an update. Am J Emerg Med. 2012, 30: 972-980. 10.1016/j.ajem.2011.06.016.CrossRefPubMed
13.
go back to reference Widmer LL, Blank PR, Van Herck K, Hatz C, Schlagenhauf P: Cost-effectiveness analysis of malaria chemoprophylaxis for travellers to West-Africa. BMC Infect Dis. 2010, 10: 279-10.1186/1471-2334-10-279.PubMedCentralCrossRefPubMed Widmer LL, Blank PR, Van Herck K, Hatz C, Schlagenhauf P: Cost-effectiveness analysis of malaria chemoprophylaxis for travellers to West-Africa. BMC Infect Dis. 2010, 10: 279-10.1186/1471-2334-10-279.PubMedCentralCrossRefPubMed
15.
go back to reference Thang H, Elsas R, Veenstra J: Airport malaria: report of a case and a brief review of the literature. Neth J Med. 2002, 60: 441-443.PubMed Thang H, Elsas R, Veenstra J: Airport malaria: report of a case and a brief review of the literature. Neth J Med. 2002, 60: 441-443.PubMed
16.
17.
18.
go back to reference Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot OJ, Moonen B: Malaria resurgence: a systematic review and assessment of its causes. Malar J. 2012, 11: 122-10.1186/1475-2875-11-122.PubMedCentralCrossRefPubMed Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot OJ, Moonen B: Malaria resurgence: a systematic review and assessment of its causes. Malar J. 2012, 11: 122-10.1186/1475-2875-11-122.PubMedCentralCrossRefPubMed
19.
go back to reference Pindolia DK, Garcia AJ, Wesolowski A, Smith DL, Buckee CO, Noor AM, Snow RW, Tatem AJ: Human movement data for malaria control and elimination strategic planning. Malar J. 2012, 11: 205-10.1186/1475-2875-11-205.PubMedCentralCrossRefPubMed Pindolia DK, Garcia AJ, Wesolowski A, Smith DL, Buckee CO, Noor AM, Snow RW, Tatem AJ: Human movement data for malaria control and elimination strategic planning. Malar J. 2012, 11: 205-10.1186/1475-2875-11-205.PubMedCentralCrossRefPubMed
20.
go back to reference Centers for Disease Control and Prevention: Local transmission of Plasmodium vivax malaria --- Virginia, 2002. MMWR Morb Mortal Wkly Rep. 2002, 51: 921-923. Centers for Disease Control and Prevention: Local transmission of Plasmodium vivax malaria --- Virginia, 2002. MMWR Morb Mortal Wkly Rep. 2002, 51: 921-923.
21.
go back to reference Centers for Disease Control and Prevention: Local transmission of Plasmodium vivax malaria --- Palm Beach County, Florida, 2003. MMWR Morb Mortal Wkly Rep. 2003, 52: 908-911. Centers for Disease Control and Prevention: Local transmission of Plasmodium vivax malaria --- Palm Beach County, Florida, 2003. MMWR Morb Mortal Wkly Rep. 2003, 52: 908-911.
22.
go back to reference Danis K, Baka A, Lenglet A, Van Bortel W, Terzaki I, Tseroni M, Detsis M, Papanikolaou E, Balaska A, Gewehr S, Dougas G, Sideroglou T, Economopoulou A, Vakalis N, Tsiodras S, Bonovas S, Kremastinou J: Autochthonous Plasmodium vivax malaria in Greece, 2011. Euro Surveill. 2011, 16: 1-5. Danis K, Baka A, Lenglet A, Van Bortel W, Terzaki I, Tseroni M, Detsis M, Papanikolaou E, Balaska A, Gewehr S, Dougas G, Sideroglou T, Economopoulou A, Vakalis N, Tsiodras S, Bonovas S, Kremastinou J: Autochthonous Plasmodium vivax malaria in Greece, 2011. Euro Surveill. 2011, 16: 1-5.
23.
go back to reference Chiyaka C, Tatem A, Cohen J, Gething P, Johnston G, Gosling R, Laxminarayan R, Hay S, Smith D: The Stability of Malaria Elimination. Science. 2013, 339: 909-910. 10.1126/science.1229509.CrossRefPubMed Chiyaka C, Tatem A, Cohen J, Gething P, Johnston G, Gosling R, Laxminarayan R, Hay S, Smith D: The Stability of Malaria Elimination. Science. 2013, 339: 909-910. 10.1126/science.1229509.CrossRefPubMed
24.
go back to reference Wijesundera MDS: Malaria outbreaks in new foci in Sri Lanka. Parasitol Today. 1988, 4: 147-50. 10.1016/0169-4758(88)90193-7.CrossRef Wijesundera MDS: Malaria outbreaks in new foci in Sri Lanka. Parasitol Today. 1988, 4: 147-50. 10.1016/0169-4758(88)90193-7.CrossRef
25.
go back to reference Tatarsky A, Aboobakar S, Cohen JM, Gopee N, Bheecarry A, Moonasar D, Phillips A a, Kahn JG, Moonen B, Smith DL, Sabot O: Preventing the reintroduction of malaria in Mauritius: a programmatic and financial assessment. PLOS ONE. 2011, 6: e23832-10.1371/journal.pone.0023832.PubMedCentralCrossRefPubMed Tatarsky A, Aboobakar S, Cohen JM, Gopee N, Bheecarry A, Moonasar D, Phillips A a, Kahn JG, Moonen B, Smith DL, Sabot O: Preventing the reintroduction of malaria in Mauritius: a programmatic and financial assessment. PLOS ONE. 2011, 6: e23832-10.1371/journal.pone.0023832.PubMedCentralCrossRefPubMed
26.
go back to reference Lepers J, Deloron P, Fontenille D, Coulanges P: Reappearnce of falciparum malaria in Central Highland Plateaux of Madagascar. Lancet. 1988, 331: 586-CrossRef Lepers J, Deloron P, Fontenille D, Coulanges P: Reappearnce of falciparum malaria in Central Highland Plateaux of Madagascar. Lancet. 1988, 331: 586-CrossRef
27.
go back to reference Le Menach A, Tatem AJ, Cohen JM, Hay SI, Randell H, Patil AP, Smith DL: Travel risk, malaria importation and malaria transmission in Zanzibar. Sci Rep. 2011, 1: 93-PubMedCentralCrossRefPubMed Le Menach A, Tatem AJ, Cohen JM, Hay SI, Randell H, Patil AP, Smith DL: Travel risk, malaria importation and malaria transmission in Zanzibar. Sci Rep. 2011, 1: 93-PubMedCentralCrossRefPubMed
28.
go back to reference Fairhurst RM, Nayyar GML, Breman JG, Hallett R, Vennerstrom JL, Duong S, Ringwald P, Wellems TE, Plowe CV, Dondorp AM: Artemisinin-resistant malaria: research challenges, opportunities, and public health implications. Am J Trop Med Hyg. 2012, 87: 231-241. 10.4269/ajtmh.2012.12-0025.PubMedCentralCrossRefPubMed Fairhurst RM, Nayyar GML, Breman JG, Hallett R, Vennerstrom JL, Duong S, Ringwald P, Wellems TE, Plowe CV, Dondorp AM: Artemisinin-resistant malaria: research challenges, opportunities, and public health implications. Am J Trop Med Hyg. 2012, 87: 231-241. 10.4269/ajtmh.2012.12-0025.PubMedCentralCrossRefPubMed
29.
go back to reference Anderson TJC, Nair S, Nkhoma S, Williams JT, Imwong M, Yi P, Socheat D, Das D, Chotivanich K, Day NPJ, White NJ, Dondorp AM: High heritability of malaria parasite clearance rate indicates a genetic basis for artemisinin resistance in western Cambodia. J Infect Dis. 2010, 201: 1326-1330. 10.1086/651562.PubMedCentralCrossRefPubMed Anderson TJC, Nair S, Nkhoma S, Williams JT, Imwong M, Yi P, Socheat D, Das D, Chotivanich K, Day NPJ, White NJ, Dondorp AM: High heritability of malaria parasite clearance rate indicates a genetic basis for artemisinin resistance in western Cambodia. J Infect Dis. 2010, 201: 1326-1330. 10.1086/651562.PubMedCentralCrossRefPubMed
30.
go back to reference Phyo AP, Nkhoma S, Stepniewska K, Ashley E, Nair S, McGready R, ler Moo C, Al-Saai S, Dondorp AM, Lwin KM, Singhasivanon P, Day NPJ, White NJ, Anderson TJC, Nosten F: Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet. 2012, 379: 1960-1966. 10.1016/S0140-6736(12)60484-X.PubMedCentralCrossRefPubMed Phyo AP, Nkhoma S, Stepniewska K, Ashley E, Nair S, McGready R, ler Moo C, Al-Saai S, Dondorp AM, Lwin KM, Singhasivanon P, Day NPJ, White NJ, Anderson TJC, Nosten F: Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet. 2012, 379: 1960-1966. 10.1016/S0140-6736(12)60484-X.PubMedCentralCrossRefPubMed
31.
go back to reference Dondorp AM, Yeung S, White L, Nguon C, Day NPJ, Socheat D, von Seidlein L: Artemisinin resistance: current status and scenarios for containment. Nature Rev Microbiol. 2010, 8: 272-280.CrossRef Dondorp AM, Yeung S, White L, Nguon C, Day NPJ, Socheat D, von Seidlein L: Artemisinin resistance: current status and scenarios for containment. Nature Rev Microbiol. 2010, 8: 272-280.CrossRef
32.
go back to reference Trape JF: The public health impact of chloroquine resistance in Africa. Am J Trop Med Hyg. 2001, 64: 12-17.PubMed Trape JF: The public health impact of chloroquine resistance in Africa. Am J Trop Med Hyg. 2001, 64: 12-17.PubMed
33.
go back to reference Mita T, Venkatesan M, Ohashi J, Culleton R, Takahashi N, Tsukahara T, Ndounga M, Dysoley L, Endo H, Hombhanje F, Ferreira MU, Plowe CV, Tanabe K: Limited geographical origin and global spread of sulfadoxine-resistant dhps alleles in Plasmodium falciparum populations. J Infect Dis. 2011, 204: 1980-1988. 10.1093/infdis/jir664.PubMedCentralCrossRefPubMed Mita T, Venkatesan M, Ohashi J, Culleton R, Takahashi N, Tsukahara T, Ndounga M, Dysoley L, Endo H, Hombhanje F, Ferreira MU, Plowe CV, Tanabe K: Limited geographical origin and global spread of sulfadoxine-resistant dhps alleles in Plasmodium falciparum populations. J Infect Dis. 2011, 204: 1980-1988. 10.1093/infdis/jir664.PubMedCentralCrossRefPubMed
34.
go back to reference Naidoo I, Roper C: Following the path of most resistance: dhps K540E dispersal in African Plasmodium falciparum. Trends Parasitol. 2010, 26: 447-456. 10.1016/j.pt.2010.05.001.CrossRefPubMed Naidoo I, Roper C: Following the path of most resistance: dhps K540E dispersal in African Plasmodium falciparum. Trends Parasitol. 2010, 26: 447-456. 10.1016/j.pt.2010.05.001.CrossRefPubMed
35.
go back to reference World Health Organization: Global report on antimalarial drug efficacy and drug resistance: 2000–2010. 2010, Geneva: WHO Press World Health Organization: Global report on antimalarial drug efficacy and drug resistance: 2000–2010. 2010, Geneva: WHO Press
36.
go back to reference Huang Z, Wu X, Garcia AJ, Fik TJ, Tatem AJ: An open-access modeled passenger flow matrix for the global air network in 2010. PLoS One. 2013, 8: e64317-10.1371/journal.pone.0064317.PubMedCentralCrossRefPubMed Huang Z, Wu X, Garcia AJ, Fik TJ, Tatem AJ: An open-access modeled passenger flow matrix for the global air network in 2010. PLoS One. 2013, 8: e64317-10.1371/journal.pone.0064317.PubMedCentralCrossRefPubMed
38.
go back to reference O’Kelly M: The location of interacting hub facilities. Transport Sci. 1986, 20: 92-106. 10.1287/trsc.20.2.92.CrossRef O’Kelly M: The location of interacting hub facilities. Transport Sci. 1986, 20: 92-106. 10.1287/trsc.20.2.92.CrossRef
40.
41.
go back to reference Gething PW, Elyazar IRF, Moyes CL, Smith DL, Battle KE, Guerra CA, Patil AP, Tatem AJ, Howes RE, Myers MF, George DB, Horby P, Wertheim HFL, Price RN, Müeller I, Baird JK, Hay SI: A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl. 2012, 6: e1814-10.1371/journal.pntd.0001814.CrossRef Gething PW, Elyazar IRF, Moyes CL, Smith DL, Battle KE, Guerra CA, Patil AP, Tatem AJ, Howes RE, Myers MF, George DB, Horby P, Wertheim HFL, Price RN, Müeller I, Baird JK, Hay SI: A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl. 2012, 6: e1814-10.1371/journal.pntd.0001814.CrossRef
42.
go back to reference Howes RE, Patil AP, Piel FB, Nyangiri O a, Kabaria CW, Gething PW, Zimmerman P a, Barnadas C, Beall CM, Gebremedhin A, Ménard D, Williams TN, Weatherall DJ, Hay SI: The global distribution of the Duffy blood group. Nat Commun. 2011, 2: 266-PubMedCentralCrossRefPubMed Howes RE, Patil AP, Piel FB, Nyangiri O a, Kabaria CW, Gething PW, Zimmerman P a, Barnadas C, Beall CM, Gebremedhin A, Ménard D, Williams TN, Weatherall DJ, Hay SI: The global distribution of the Duffy blood group. Nat Commun. 2011, 2: 266-PubMedCentralCrossRefPubMed
43.
go back to reference Gething PW, Van Boeckel TP, Smith DL, Guerra CA, Patil AP, Snow RW, Hay SI: Modelling the global constraints of temperature on transmission of Plasmodium falciparum and P. vivax. Parasit Vectors. 2011, 4: 92-10.1186/1756-3305-4-92.PubMedCentralCrossRefPubMed Gething PW, Van Boeckel TP, Smith DL, Guerra CA, Patil AP, Snow RW, Hay SI: Modelling the global constraints of temperature on transmission of Plasmodium falciparum and P. vivax. Parasit Vectors. 2011, 4: 92-10.1186/1756-3305-4-92.PubMedCentralCrossRefPubMed
45.
go back to reference Freeman L: A set of measures of centrality based on betweenness. Sociometry. 1977, 40: 35-41. 10.2307/3033543.CrossRef Freeman L: A set of measures of centrality based on betweenness. Sociometry. 1977, 40: 35-41. 10.2307/3033543.CrossRef
46.
go back to reference Barrat A, Barthélemy M, Pastor-Satorras R, Vespignani A: The architecture of complex weighted networks. Proc Natl Acad Sci. 2004, 101: 3747-3752. 10.1073/pnas.0400087101.PubMedCentralCrossRefPubMed Barrat A, Barthélemy M, Pastor-Satorras R, Vespignani A: The architecture of complex weighted networks. Proc Natl Acad Sci. 2004, 101: 3747-3752. 10.1073/pnas.0400087101.PubMedCentralCrossRefPubMed
47.
go back to reference Guimerà R, Mossa S, Turtschi A, Amaral L: The worldwide air transportation network: Anomalous centrality, community structure, and cities’ global roles. Proc Natl Acad Sci. 2005, 102: 7794-7799. 10.1073/pnas.0407994102.PubMedCentralCrossRefPubMed Guimerà R, Mossa S, Turtschi A, Amaral L: The worldwide air transportation network: Anomalous centrality, community structure, and cities’ global roles. Proc Natl Acad Sci. 2005, 102: 7794-7799. 10.1073/pnas.0407994102.PubMedCentralCrossRefPubMed
48.
go back to reference Brandes U: A faster algorithm for betweenness centrality. J Math Sociol. 2001, 25: 163-177. 10.1080/0022250X.2001.9990249.CrossRef Brandes U: A faster algorithm for betweenness centrality. J Math Sociol. 2001, 25: 163-177. 10.1080/0022250X.2001.9990249.CrossRef
49.
go back to reference Fortunato S: Community detection in graphs. Phys Rep. 2010, 486: 75-174. 10.1016/j.physrep.2009.11.002.CrossRef Fortunato S: Community detection in graphs. Phys Rep. 2010, 486: 75-174. 10.1016/j.physrep.2009.11.002.CrossRef
50.
go back to reference Tatem AJ, Smith DL: International population movements and regional Plasmodium falciparum malaria elimination strategies. Proc Natl Acad Sci. 2010, 107: 12222-12227. 10.1073/pnas.1002971107.PubMedCentralCrossRefPubMed Tatem AJ, Smith DL: International population movements and regional Plasmodium falciparum malaria elimination strategies. Proc Natl Acad Sci. 2010, 107: 12222-12227. 10.1073/pnas.1002971107.PubMedCentralCrossRefPubMed
51.
go back to reference Wesolowski A, Eagle N, Tatem AJ, Smith DL, Noor AM, Snow RW, Buckee CO: Quantifying the impact of human mobility on malaria. Science. 2012, 338: 267-270. 10.1126/science.1223467.PubMedCentralCrossRefPubMed Wesolowski A, Eagle N, Tatem AJ, Smith DL, Noor AM, Snow RW, Buckee CO: Quantifying the impact of human mobility on malaria. Science. 2012, 338: 267-270. 10.1126/science.1223467.PubMedCentralCrossRefPubMed
52.
53.
go back to reference Blondel V, Guillaume J: Fast unfolding of communities in large networks. J Stat Mech Theor Exp. 2008, 2008: 1-12.CrossRef Blondel V, Guillaume J: Fast unfolding of communities in large networks. J Stat Mech Theor Exp. 2008, 2008: 1-12.CrossRef
54.
go back to reference Bauer D: Constructing confidence sets using rank statistics. J Amer Statist Assoc. 1972, 67: 687-690. 10.1080/01621459.1972.10481279.CrossRef Bauer D: Constructing confidence sets using rank statistics. J Amer Statist Assoc. 1972, 67: 687-690. 10.1080/01621459.1972.10481279.CrossRef
55.
go back to reference UCSF Global Health Group: Atlas of Malaria-Eliminating Countries. 2011, San Francisco: Global Health Sciences UCSF Global Health Group: Atlas of Malaria-Eliminating Countries. 2011, San Francisco: Global Health Sciences
56.
go back to reference Talisuna A, Karema C, Ogutu B: Mitigating the threat of artemisinin resistance in Africa: improvement of drug-resistance surveillance and response systems. Lancet Infect Dis. 2012, 12: 888-896. 10.1016/S1473-3099(12)70241-4.PubMedCentralCrossRefPubMed Talisuna A, Karema C, Ogutu B: Mitigating the threat of artemisinin resistance in Africa: improvement of drug-resistance surveillance and response systems. Lancet Infect Dis. 2012, 12: 888-896. 10.1016/S1473-3099(12)70241-4.PubMedCentralCrossRefPubMed
57.
go back to reference O’Meara WP, Mangeni JN, Steketee R, Greenwood B: Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis. 2010, 10: 545-555. 10.1016/S1473-3099(10)70096-7.CrossRefPubMed O’Meara WP, Mangeni JN, Steketee R, Greenwood B: Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis. 2010, 10: 545-555. 10.1016/S1473-3099(10)70096-7.CrossRefPubMed
58.
go back to reference Brons M, Pels E, Nijkamp P, Rietveld P: Price elasticities of demand for passenger air travel: a meta-analysis. J Air Transp Manag. 2002, 8: 165-175. 10.1016/S0969-6997(01)00050-3.CrossRef Brons M, Pels E, Nijkamp P, Rietveld P: Price elasticities of demand for passenger air travel: a meta-analysis. J Air Transp Manag. 2002, 8: 165-175. 10.1016/S0969-6997(01)00050-3.CrossRef
59.
go back to reference Tatem AJ, Qiu Y, Smith DL, Sabot O, Ali AS, Moonen B: The use of mobile phone data for the estimation of the travel patterns and imported Plasmodium falciparum rates among Zanzibar residents. Malar J. 2009, 8: 287-10.1186/1475-2875-8-287.PubMedCentralCrossRefPubMed Tatem AJ, Qiu Y, Smith DL, Sabot O, Ali AS, Moonen B: The use of mobile phone data for the estimation of the travel patterns and imported Plasmodium falciparum rates among Zanzibar residents. Malar J. 2009, 8: 287-10.1186/1475-2875-8-287.PubMedCentralCrossRefPubMed
60.
go back to reference Johansson MA, Arana-Vizcarrondo N, Biggerstaff BJ, Gallagher N, Marano N, Staples JE: Assessing the risk of international spread of yellow fever virus: a mathematical analysis of an urban outbreak in Asuncion, 2008. AmJTrop Med Hyg. 2012, 86: 349-358. 10.4269/ajtmh.2012.11-0432.CrossRef Johansson MA, Arana-Vizcarrondo N, Biggerstaff BJ, Gallagher N, Marano N, Staples JE: Assessing the risk of international spread of yellow fever virus: a mathematical analysis of an urban outbreak in Asuncion, 2008. AmJTrop Med Hyg. 2012, 86: 349-358. 10.4269/ajtmh.2012.11-0432.CrossRef
62.
go back to reference Hay SI, Guerra CA, Tatem AJ, Noor AM, Snow RW: Reviews The global distribution and population at risk of malaria : past, present, and future. Lancet. 2004, 4: 327-336.PubMedCentralCrossRefPubMed Hay SI, Guerra CA, Tatem AJ, Noor AM, Snow RW: Reviews The global distribution and population at risk of malaria : past, present, and future. Lancet. 2004, 4: 327-336.PubMedCentralCrossRefPubMed
64.
go back to reference Tatem AJ, Hemelaar J, Gray R, Salemi M: Spatial accessibility and the spread of HIV-1 subtypes and recombinants in sub-Saharan Africa. AIDS. 2012, 26: 2351-2360. 10.1097/QAD.0b013e328359a904.CrossRefPubMed Tatem AJ, Hemelaar J, Gray R, Salemi M: Spatial accessibility and the spread of HIV-1 subtypes and recombinants in sub-Saharan Africa. AIDS. 2012, 26: 2351-2360. 10.1097/QAD.0b013e328359a904.CrossRefPubMed
65.
go back to reference Linard C, Gilbert M, Snow RW, Noor AM, Tatem AJ: Population distribution, settlement patterns and accessibility across Africa in 2010. PLoS One. 2012, 7: e31743-10.1371/journal.pone.0031743.PubMedCentralCrossRefPubMed Linard C, Gilbert M, Snow RW, Noor AM, Tatem AJ: Population distribution, settlement patterns and accessibility across Africa in 2010. PLoS One. 2012, 7: e31743-10.1371/journal.pone.0031743.PubMedCentralCrossRefPubMed
66.
go back to reference Cohen J, Woolsey A, Sabot O: Optimizing investments in malaria treatment and diagnosis. Science. 2012, 338: 612-614. 10.1126/science.1229045.CrossRefPubMed Cohen J, Woolsey A, Sabot O: Optimizing investments in malaria treatment and diagnosis. Science. 2012, 338: 612-614. 10.1126/science.1229045.CrossRefPubMed
67.
go back to reference Flegg JA, Guerin PJ, White NJ, Stepniewska K: Standardizing the measurement of parasite clearance in falciparum malaria: the parasite clearance estimator. Malar J. 2011, 10: 339-10.1186/1475-2875-10-339.PubMedCentralCrossRefPubMed Flegg JA, Guerin PJ, White NJ, Stepniewska K: Standardizing the measurement of parasite clearance in falciparum malaria: the parasite clearance estimator. Malar J. 2011, 10: 339-10.1186/1475-2875-10-339.PubMedCentralCrossRefPubMed
Metadata
Title
Global malaria connectivity through air travel
Authors
Zhuojie Huang
Andrew J Tatem
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2013
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-12-269

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