Population-level mathematical modeling of antimicrobial resistance: a systematic review.
Antimicrobial
Communicable diseases
Computational
Epidemiology
Mathematical
Models
Resistance
Transmission
Journal
BMC medicine
ISSN: 1741-7015
Titre abrégé: BMC Med
Pays: England
ID NLM: 101190723
Informations de publication
Date de publication:
24 04 2019
24 04 2019
Historique:
received:
17
12
2018
accepted:
25
03
2019
entrez:
25
4
2019
pubmed:
25
4
2019
medline:
14
11
2019
Statut:
epublish
Résumé
Mathematical transmission models are increasingly used to guide public health interventions for infectious diseases, particularly in the context of emerging pathogens; however, the contribution of modeling to the growing issue of antimicrobial resistance (AMR) remains unclear. Here, we systematically evaluate publications on population-level transmission models of AMR over a recent period (2006-2016) to gauge the state of research and identify gaps warranting further work. We performed a systematic literature search of relevant databases to identify transmission studies of AMR in viral, bacterial, and parasitic disease systems. We analyzed the temporal, geographic, and subject matter trends, described the predominant medical and behavioral interventions studied, and identified central findings relating to key pathogens. We identified 273 modeling studies; the majority of which (> 70%) focused on 5 infectious diseases (human immunodeficiency virus (HIV), influenza virus, Plasmodium falciparum (malaria), Mycobacterium tuberculosis (TB), and methicillin-resistant Staphylococcus aureus (MRSA)). AMR studies of influenza and nosocomial pathogens were mainly set in industrialized nations, while HIV, TB, and malaria studies were heavily skewed towards developing countries. The majority of articles focused on AMR exclusively in humans (89%), either in community (58%) or healthcare (27%) settings. Model systems were largely compartmental (76%) and deterministic (66%). Only 43% of models were calibrated against epidemiological data, and few were validated against out-of-sample datasets (14%). The interventions considered were primarily the impact of different drug regimens, hygiene and infection control measures, screening, and diagnostics, while few studies addressed de novo resistance, vaccination strategies, economic, or behavioral changes to reduce antibiotic use in humans and animals. The AMR modeling literature concentrates on disease systems where resistance has been long-established, while few studies pro-actively address recent rise in resistance in new pathogens or explore upstream strategies to reduce overall antibiotic consumption. Notable gaps include research on emerging resistance in Enterobacteriaceae and Neisseria gonorrhoeae; AMR transmission at the animal-human interface, particularly in agricultural and veterinary settings; transmission between hospitals and the community; the role of environmental factors in AMR transmission; and the potential of vaccines to combat AMR.
Sections du résumé
BACKGROUND
Mathematical transmission models are increasingly used to guide public health interventions for infectious diseases, particularly in the context of emerging pathogens; however, the contribution of modeling to the growing issue of antimicrobial resistance (AMR) remains unclear. Here, we systematically evaluate publications on population-level transmission models of AMR over a recent period (2006-2016) to gauge the state of research and identify gaps warranting further work.
METHODS
We performed a systematic literature search of relevant databases to identify transmission studies of AMR in viral, bacterial, and parasitic disease systems. We analyzed the temporal, geographic, and subject matter trends, described the predominant medical and behavioral interventions studied, and identified central findings relating to key pathogens.
RESULTS
We identified 273 modeling studies; the majority of which (> 70%) focused on 5 infectious diseases (human immunodeficiency virus (HIV), influenza virus, Plasmodium falciparum (malaria), Mycobacterium tuberculosis (TB), and methicillin-resistant Staphylococcus aureus (MRSA)). AMR studies of influenza and nosocomial pathogens were mainly set in industrialized nations, while HIV, TB, and malaria studies were heavily skewed towards developing countries. The majority of articles focused on AMR exclusively in humans (89%), either in community (58%) or healthcare (27%) settings. Model systems were largely compartmental (76%) and deterministic (66%). Only 43% of models were calibrated against epidemiological data, and few were validated against out-of-sample datasets (14%). The interventions considered were primarily the impact of different drug regimens, hygiene and infection control measures, screening, and diagnostics, while few studies addressed de novo resistance, vaccination strategies, economic, or behavioral changes to reduce antibiotic use in humans and animals.
CONCLUSIONS
The AMR modeling literature concentrates on disease systems where resistance has been long-established, while few studies pro-actively address recent rise in resistance in new pathogens or explore upstream strategies to reduce overall antibiotic consumption. Notable gaps include research on emerging resistance in Enterobacteriaceae and Neisseria gonorrhoeae; AMR transmission at the animal-human interface, particularly in agricultural and veterinary settings; transmission between hospitals and the community; the role of environmental factors in AMR transmission; and the potential of vaccines to combat AMR.
Identifiants
pubmed: 31014341
doi: 10.1186/s12916-019-1314-9
pii: 10.1186/s12916-019-1314-9
pmc: PMC6480522
doi:
Substances chimiques
Anti-Bacterial Agents
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
81Subventions
Organisme : NICHD NIH HHS
ID : P2C HD047879
Pays : United States
Références
Nature. 2006 Nov 23;444 Suppl 1:9-18
pubmed: 17159890
Health Aff (Millwood). 2006 Mar-Apr;25(2):325-36
pubmed: 16522574
J Infect Dis. 2008 Nov 15;198(10):1502-13
pubmed: 18816192
Ann N Y Acad Sci. 2019 Jan;1436(1):157-173
pubmed: 30120891
Math Biosci Eng. 2010 Oct;7(4):779-92
pubmed: 21077707
Science. 2006 Apr 21;312(5772):389-91
pubmed: 16627735
Curr Opin Infect Dis. 2011 Jun;24(3):279-87
pubmed: 21467930
J Biol Dyn. 2010 Jan;4(1):115-29
pubmed: 19587839
PLoS Comput Biol. 2010 Mar 19;6(3):e1000715
pubmed: 20333236
Biometrics. 2008 Sep;64(3):851-9
pubmed: 18047536
Infect Control Hosp Epidemiol. 2013 Feb;34(2):151-60
pubmed: 23295561
Aust N Z J Public Health. 2014 Feb;38(1):78-82
pubmed: 24494951
Proc Natl Acad Sci U S A. 2006 May 2;103(18):7042-7
pubmed: 16632605
Epidemiol Infect. 2008 Dec;136(12):1585-98
pubmed: 18606028
PLoS Comput Biol. 2012;8(4):e1002454
pubmed: 22511854
Sci Transl Med. 2013 Apr 10;5(180):180ra49
pubmed: 23576815
PLoS One. 2013 Aug 01;8(8):e70499
pubmed: 23936442
PLoS One. 2015 Jul 01;10(7):e0131438
pubmed: 26132584
PLoS One. 2016 Jul 08;11(7):e0158620
pubmed: 27391094
AIDS. 2011 Mar 27;25(6):843-50
pubmed: 21192233
BMC Infect Dis. 2013 Jun 28;13:294
pubmed: 23809195
J R Soc Interface. 2012 Apr 7;9(69):648-56
pubmed: 21865253
Malar J. 2008 Nov 02;7:229
pubmed: 18976503
PLoS Comput Biol. 2011 Apr;7(4):e1002026
pubmed: 21552544
PLoS One. 2010 Jun 08;5(6):e10981
pubmed: 20544022
PLoS Comput Biol. 2011 Mar;7(3):e1001094
pubmed: 21390265
Epidemiol Infect. 2010 Jun;138(6):873-83
pubmed: 19796449
Epidemiol Infect. 2008 Mar;136(3):289-98
pubmed: 17767792
Biostatistics. 2007 Apr;8(2):383-401
pubmed: 16926230
Prev Vet Med. 2007 May 16;79(2-4):186-203
pubmed: 17270298
PLoS One. 2013 Jul 25;8(7):e68940
pubmed: 23935910
J Hosp Infect. 2016 Aug;93(4):395-402
pubmed: 26944903
Math Biosci. 2015 May;263:121-32
pubmed: 25726716
Bull World Health Organ. 2015 Nov 1;93(11):790-8
pubmed: 26549907
PLoS One. 2009;4(3):e4915
pubmed: 19295921
Clin Infect Dis. 2009 Feb 1;48(3):274-84
pubmed: 19137654
Bull Math Biol. 2009 Jan;71(1):247-63
pubmed: 19082663
J Virol. 2012 May;86(10):5885-94
pubmed: 22438533
Infect Control Hosp Epidemiol. 2011 Jun;32(6):562-72
pubmed: 21558768
J R Soc Interface. 2016 Dec;13(125):
pubmed: 28003528
Crit Care Med. 2015 Feb;43(2):382-93
pubmed: 25377019
Proc Natl Acad Sci U S A. 2006 Jun 20;103(25):9655-60
pubmed: 16772381
PLoS One. 2007 Jan 17;2(1):e152
pubmed: 17225857
BMC Infect Dis. 2009 Jan 22;9:8
pubmed: 19161634
Infect Control Hosp Epidemiol. 2011 Nov;32(11):1073-8
pubmed: 22011533
mBio. 2016 Jun 07;7(3):
pubmed: 27273824
PLoS One. 2015 Jul 16;10(7):e0133202
pubmed: 26181042
Foodborne Pathog Dis. 2007 Fall;4(3):313-26
pubmed: 17883315
Proc Biol Sci. 2013 Jun 19;280(1764):20130519
pubmed: 23782877
Vet Sci. 2018 Apr 08;5(2):
pubmed: 29642473
Eur J Microbiol Immunol (Bp). 2011 Sep;1(3):190-7
pubmed: 24516724
Clin Microbiol Infect. 2011 Nov;17(11):1717-26
pubmed: 21595796
Eur Respir J. 2010 Oct;36(4):870-7
pubmed: 20351030
Proc Natl Acad Sci U S A. 2006 Apr 4;103(14):5620-5
pubmed: 16565219
PLoS Comput Biol. 2013;9(2):e1002874
pubmed: 23436984
J Theor Biol. 2010 Jun 7;264(3):645-56
pubmed: 20347850
PLoS Comput Biol. 2013;9(11):e1003328
pubmed: 24277998
J Infect Dis. 2008 Jul 1;198(1):59-67
pubmed: 18498241
Rev Sci Tech. 2011 Aug;30(2):547-54
pubmed: 21961225
Rev Esp Quimioter. 2015 Feb;28(1):10-20
pubmed: 25690140
Genetics. 2014 Dec;198(4):1395-404
pubmed: 25313129
Prev Vet Med. 2011 May 1;99(2-4):211-24
pubmed: 21277032
Int J Infect Dis. 2012 Oct;16(10):e739-47
pubmed: 22818291
Antimicrob Agents Chemother. 2013 Sep;57(9):4410-6
pubmed: 23817383
Mar Drugs. 2017 Jun 01;15(6):
pubmed: 28587172
Infect Control Hosp Epidemiol. 2016 Nov;37(11):1315-1322
pubmed: 27609341
PLoS Comput Biol. 2006 Oct;2(10):e137
pubmed: 17040124
J Biol Dyn. 2017 Mar;11(sup1):65-78
pubmed: 26916119
BMC Infect Dis. 2017 Sep 11;17(1):612
pubmed: 28893198
Open Forum Infect Dis. 2014 Aug 30;1(2):ofu073
pubmed: 25734143
Clin Lab Sci. 2009 Winter;22(1):26-9
pubmed: 19354025
Vet Parasitol. 2012 Jun 8;187(1-2):285-94
pubmed: 22244532
BMC Infect Dis. 2013 Dec 17;13:595
pubmed: 24341774
J Biol Dyn. 2012;6:645-62
pubmed: 22873610
J Theor Biol. 2011 Nov 7;288:9-20
pubmed: 21840324
J Theor Biol. 2012 Jan 21;293:161-73
pubmed: 22024632
Science. 2015 Mar 13;347(6227):aaa4339
pubmed: 25766240
Epidemics. 2015 Mar;10:45-8
pubmed: 25843382
Sci Rep. 2011;1:185
pubmed: 22355700
Int J Parasitol Drugs Drug Resist. 2016 Dec;6(3):258-271
pubmed: 27915061
PLoS One. 2012;7(1):e29757
pubmed: 22238650
J Biol Dyn. 2013;7:133-47
pubmed: 23859002
Proc Biol Sci. 2014 Feb 12;281(1780):20133172
pubmed: 24523276
J Am Med Dir Assoc. 2012 Jul;13(6):568.e1-13
pubmed: 22575772
Influenza Other Respir Viruses. 2013 Jan;7 Suppl 1:58-62
pubmed: 23279898
PLoS One. 2015 May 04;10(5):e0126267
pubmed: 25938501
Open Forum Infect Dis. 2016 Jun 16;3(3):ofw125
pubmed: 27703992
J Antimicrob Chemother. 2015 Dec;70(12):3366-78
pubmed: 26338047
Epidemics. 2012 Dec;4(4):203-10
pubmed: 23351372
J Theor Biol. 2007 Apr 7;245(3):470-81
pubmed: 17188714
Theor Popul Biol. 2007 Mar;71(2):196-212
pubmed: 17174368
BMC Infect Dis. 2013 Sep 30;13:449
pubmed: 24073821
Proc Natl Acad Sci U S A. 2009 May 5;106(18):7672-7
pubmed: 19365076
Travel Med Infect Dis. 2018 Mar - Apr;22:8-17
pubmed: 29482014
Stat Commun Infect Dis. 2010 Jan;2(1):1012
pubmed: 24490001
BMC Infect Dis. 2014 Dec 06;14:634
pubmed: 25480675
Biosystems. 2014 May;119:20-44
pubmed: 24704209
Trends Microbiol. 2014 Jan;22(1):36-41
pubmed: 24289955
J Infect Dis. 2006 May 15;193(10):1473-4
pubmed: 16619199
J Am Med Dir Assoc. 2016 Feb;17(2):183.e1-16
pubmed: 26778488
Curr Opin HIV AIDS. 2011 Mar;6(2):131-40
pubmed: 21505388
Biol Lett. 2015 Nov;11(11):
pubmed: 26601680
Epidemics. 2015 Mar;10:21-5
pubmed: 25843377
Trop Med Int Health. 2011 Mar;16(3):368-74
pubmed: 21138508
Math Biosci. 2014 Mar;249:8-17
pubmed: 24480735
J Clin Microbiol. 2009 May;47(5):1484-90
pubmed: 19297604
Comput Methods Programs Biomed. 2011 Nov;104(2):260-5
pubmed: 21377229
J R Soc Interface. 2007 Oct 22;4(16):893-906
pubmed: 17609176
J Hosp Infect. 2013 Sep;85(1):33-44
pubmed: 23911111
Epidemiol Infect. 2007 Feb;135(2):328-42
pubmed: 16836799
J Antimicrob Chemother. 2016 May;71(5):1367-79
pubmed: 26869689
Am J Epidemiol. 2013 Jun 1;177(11):1306-13
pubmed: 23592544
J Theor Biol. 2007 Sep 7;248(1):179-93
pubmed: 17582443
Vet Parasitol. 2016 Aug 15;226:174-88
pubmed: 27514904
J Infect Dis. 2016 Dec 1;214(suppl_4):S375-S379
pubmed: 28830113
Malar J. 2007 Jan 22;6:9
pubmed: 17241476
J Wildl Dis. 2015 Oct;51(4):811-20
pubmed: 26221860
Infect Control Hosp Epidemiol. 2010 Jun;31(6):598-606
pubmed: 20402588
Epidemics. 2012 Dec;4(4):171-8
pubmed: 23351369
Sex Transm Infect. 2015 Jun;91(4):300-2
pubmed: 25512669
Int J Tuberc Lung Dis. 2009 May;13(5):652-8
pubmed: 19383201
Math Med Biol. 2011 Dec;28(4):335-55
pubmed: 20884768
Front Microbiol. 2013 Jul 11;4:193
pubmed: 23874327
Math Biosci. 2016 Jan;271:42-61
pubmed: 26519788
Infect Control Hosp Epidemiol. 2016 Mar;37(3):272-80
pubmed: 26708383
BMC Infect Dis. 2012 Nov 14;12:302
pubmed: 23151152
Infect Control Hosp Epidemiol. 2015 Jan;36(1):17-27
pubmed: 25627757
Sci Rep. 2015 Mar 25;5:9478
pubmed: 25804674
PLoS One. 2008 Jun 04;3(6):e2362
pubmed: 18523549
Nature. 2003 Dec 11;426(6967):658-61
pubmed: 14668863
PLoS One. 2012;7(5):e37166
pubmed: 22662135
Expert Rev Respir Med. 2009 Feb;3(1):67-79
pubmed: 20477283
Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):13980-5
pubmed: 19666590
Lancet Infect Dis. 2016 Mar;16(3):348-56
pubmed: 26616206
Emerg Infect Dis. 2013 Nov;19(11):1797-1802
pubmed: 24207050
J Theor Biol. 2011 Jul 7;280(1):88-100
pubmed: 21514304
Malar J. 2014 Sep 24;13:380
pubmed: 25249272
AIDS. 2014 Jan 2;28(1):73-83
pubmed: 23921620
Med Decis Making. 2010 Jul-Aug;30(4):E64-81
pubmed: 20634545
PLoS One. 2011 Apr 15;6(4):e18165
pubmed: 21525976
PLoS One. 2014 May 01;9(5):e96308
pubmed: 24788143
Malar J. 2009 Feb 20;8:31
pubmed: 19228438
J Infect Dis. 2013 Jul 15;208(2):224-34
pubmed: 23570850
PLoS One. 2011 Feb 16;6(2):e17038
pubmed: 21359229
Lancet Respir Med. 2015 Dec;3(12):963-72
pubmed: 26597127
Epidemiol Infect. 2015 Jun;143(8):1575-84
pubmed: 25275435
Antimicrob Resist Infect Control. 2016 Sep 22;5:32
pubmed: 27688877
PLoS Pathog. 2016 May 19;12(5):e1005611
pubmed: 27196299
Am J Epidemiol. 2008 Sep 1;168(5):548-57
pubmed: 18635575
Stat Med. 2008 Dec 30;27(30):6522-31
pubmed: 18759371
Nat Med. 2018 Jan 9;24(1):10-19
pubmed: 29315295
PLoS One. 2008 Jun 04;3(6):e2363
pubmed: 18523659
PLoS Med. 2009 May 19;6(5):e1000085
pubmed: 19440354
Clin Microbiol Rev. 2013 Jan;26(1):36-57
pubmed: 23297258
J R Soc Interface. 2010 Sep 6;7(50):1247-56
pubmed: 20504800
Trop Med Infect Dis. 2017 Oct 15;2(4):
pubmed: 30270911
BMC Med. 2009 Dec 02;7:73
pubmed: 19954514
BMC Infect Dis. 2013 Apr 24;13:187
pubmed: 23618041
Lancet. 2011 Jan 15;377(9761):228-41
pubmed: 21146207
Proc Natl Acad Sci U S A. 2014 Mar 4;111(9):3556-60
pubmed: 24550476
Ups J Med Sci. 2014 May;119(2):113-6
pubmed: 24697355
Proc Biol Sci. 2008 May 22;275(1639):1163-9
pubmed: 18270154
Sci Transl Med. 2012 May 23;4(135):135ra67
pubmed: 22623743
Comput Math Methods Med. 2012;2012:605861
pubmed: 22291852
Sex Transm Infect. 2012 Apr;88(3):200-4
pubmed: 22169277
Epidemics. 2012 Dec;4(4):219-26
pubmed: 23351374
J Theor Biol. 2009 Jul 21;259(2):253-63
pubmed: 19344730
PLoS One. 2012;7(12):e50688
pubmed: 23227198
Antimicrob Resist Infect Control. 2017 May 15;6:47
pubmed: 28515903
Int J Tuberc Lung Dis. 2015 Sep;19(9):1115-24, i-xv
pubmed: 26260835
Annu Rev Public Health. 2008;29:151-69
pubmed: 18348709
PLoS One. 2012;7(2):e30170
pubmed: 22363420
Proc Natl Acad Sci U S A. 2010 Jul 6;107(27):12381-6
pubmed: 20616092
Environ Sci Technol. 2012 Nov 6;46(21):11541-9
pubmed: 23035771
Emerg Infect Dis. 2009 Oct;15(10):1547-55
pubmed: 19861044
BMC Public Health. 2010 Jun 21;10:355
pubmed: 20565947
J Int AIDS Soc. 2014 Dec 05;17:19164
pubmed: 25491351
Trends Parasitol. 2009 May;25(5):220-7
pubmed: 19349210
Clin Infect Dis. 2015 Nov 1;61 Suppl 4:S251-8
pubmed: 26449939
Med Care. 2013 Mar;51(3):205-15
pubmed: 23358388
Nat Rev Microbiol. 2015 May;13(5):310-7
pubmed: 25817583
AIDS. 2013 Nov 28;27(18):2943-51
pubmed: 23939237
Math Model Nat Phenom. 2010;5(3):76-73
pubmed: 20740067
Clin Infect Dis. 2013 Jun;56(12):1789-96
pubmed: 23487387
Proc Natl Acad Sci U S A. 2009 Aug 25;106(34):14711-5
pubmed: 19706556
Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9835-40
pubmed: 18606986
Lancet Infect Dis. 2006 Jan;6(1):39-45
pubmed: 16377533
PLoS One. 2011;6(7):e20604
pubmed: 21750700
J Antimicrob Chemother. 2012 Jul;67(7):1775-80
pubmed: 22523315
Proc Natl Acad Sci U S A. 2008 Aug 12;105(32):11293-8
pubmed: 18695217
PLoS One. 2015 Jul 21;10(7):e0132586
pubmed: 26197056
Antimicrob Agents Chemother. 2010 Jun;54(6):2330-7
pubmed: 20231396
Antimicrob Resist Infect Control. 2018 Sep 29;7:117
pubmed: 30288257
PLoS Pathog. 2013 Feb;9(2):e1003134
pubmed: 23468619
PLoS One. 2016 Dec 1;11(12):e0165614
pubmed: 27906986
Clin Infect Dis. 2012 Jun;54(11):1618-20
pubmed: 22491330
F1000Res. 2018 Feb 15;7:193
pubmed: 29511533
J Evol Biol. 2014 Dec;27(12):2595-604
pubmed: 25417787
AIDS. 2014 Jan;28 Suppl 1:S15-23
pubmed: 24468943
AIDS. 2016 Nov 13;30(17):2715-2723
pubmed: 27782966
Epidemiol Infect. 2014 Feb;142(2):358-70
pubmed: 23676258
Math Biosci. 2013 Jan;241(1):115-24
pubmed: 23103300
PLoS Med. 2006 May;3(5):e141
pubmed: 16573365
PLoS Med. 2006 Jul;3(7):e241
pubmed: 16796403
BMC Infect Dis. 2009 May 15;9:64
pubmed: 19445655
Epidemiol Infect. 2014 Mar;142(3):468-78
pubmed: 23701989
Lancet Infect Dis. 2016 Jul;16(7):e127-e133
pubmed: 27083976
Epidemiol Infect. 1998 Jun;120(3):281-95
pubmed: 9692607
Lancet. 2007 Oct 27;370(9597):1500-7
pubmed: 17964351
J Epidemiol Community Health. 2011 Jan;65(1):87-94
pubmed: 20966445
Antimicrob Agents Chemother. 2011 Nov;55(11):5255-61
pubmed: 21788454
Front Microbiol. 2016 Oct 18;7:1626
pubmed: 27803693
Theor Biol Med Model. 2012 Jun 27;9:25
pubmed: 22738359
Antimicrob Agents Chemother. 2011 Oct;55(10):4888-95
pubmed: 21788461
Clin Infect Dis. 2015 Oct 15;61Suppl 3:S147-54
pubmed: 26409276
J Hosp Infect. 2009 Dec;73(4):364-70
pubmed: 19786313
Math Biosci Eng. 2008 Jul;5(3):437-55
pubmed: 18616351
Microb Drug Resist. 2006 Fall;12(3):149-57
pubmed: 17002540
Infect Genet Evol. 2016 Dec;46:233-240
pubmed: 27530215
Exp Biol Med (Maywood). 2011 Aug;236(8):955-61
pubmed: 21727183
Epidemiol Infect. 2016 Jul;144(9):1974-82
pubmed: 26838136
J Math Biol. 2016 Dec;73(6-7):1353-1378
pubmed: 27032641
Lancet Infect Dis. 2014 Oct;14(10):982-91
pubmed: 25213732
PLoS One. 2012;7(1):e29407
pubmed: 22272234
Am J Epidemiol. 2016 Jun 15;183(12):1138-48
pubmed: 27199387
Geospat Health. 2010 May;4(2):201-17
pubmed: 20503189
Emerg Infect Dis. 2000 May-Jun;6(3):228-37
pubmed: 10827112
Proc Biol Sci. 2007 Jul 22;274(1619):1675-84
pubmed: 17507331
Antivir Ther. 2004 Feb;9(1):57-65
pubmed: 15040537
J R Soc Interface. 2011 Apr 6;8(57):578-84
pubmed: 20861037
PLoS One. 2016 Sep 30;11(9):e0163880
pubmed: 27690247
Nat Clim Chang. 2018 Jun;8(6):510-514
pubmed: 30369964
Int J Med Microbiol. 2016 Nov;306(7):566-571
pubmed: 27345493
J Theor Biol. 2014 Oct 7;358:74-84
pubmed: 24878110
PLoS One. 2008 Mar 19;3(3):e1839
pubmed: 18350174
Am J Infect Control. 2013 Aug;41(8):668-73
pubmed: 23896284
Virulence. 2016;7(2):141-52
pubmed: 26252184
Clin Infect Dis. 2016 Mar 1;62(5):631-6
pubmed: 26658054
J R Soc Interface. 2012 Oct 7;9(75):2639-52
pubmed: 22572025
PLoS Med. 2007 Jan;4(1):e15
pubmed: 17253900
Epidemics. 2009 Sep;1(3):185-95
pubmed: 20161493
PLoS One. 2013;8(3):e59549
pubmed: 23527217
PLoS One. 2013;8(3):e59529
pubmed: 23555694
Lancet Glob Health. 2017 Dec;5(12):e1176-e1177
pubmed: 29128252
Nat Rev Microbiol. 2007 Sep;5(9):700-9
pubmed: 17703226
J Antimicrob Chemother. 2012 Jun;67(6):1325-32
pubmed: 22378682