Molecular aspects of Rift Valley fever virus and the emergence of reassortants.


Journal

Virus genes
ISSN: 1572-994X
Titre abrégé: Virus Genes
Pays: United States
ID NLM: 8803967

Informations de publication

Date de publication:
Feb 2019
Historique:
received: 22 02 2018
accepted: 03 11 2018
pubmed: 15 11 2018
medline: 23 2 2019
entrez: 15 11 2018
Statut: ppublish

Résumé

Rift Valley fever phlebovirus (RVFV) is a mosquito-transmitted pathogen endemic to sub-Saharan Africa and the Arabian Peninsula. RVFV is a threat to both animal and human health and has costly economic consequences mainly related to livestock production and trade. Competent hosts and vectors for RVFV are widespread, existing outside of endemic countries including the USA. Thus, the possibility of RVFV spreading to the USA or other countries worldwide is of significant concern. RVFV (genus Phlebovirus) is comprised of an enveloped virion containing a three-segmented, negative-stranded RNA genome that is able to undergo genetic reassortment. Reassortment has the potential to produce viruses that are more pathogenic, easily transmissible, and that have wider vector or host range. This is especially concerning because of the wide use of live attenuated vaccine strains throughout endemic countries. This review focuses on the molecular aspects of RVFV, genetic diversity of RVFV strains, and RVFV reassortment.

Identifiants

pubmed: 30426314
doi: 10.1007/s11262-018-1611-y
pii: 10.1007/s11262-018-1611-y
doi:

Substances chimiques

RNA, Viral 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

1-11

Références

Ikegami T, Makino S (2011) The pathogenesis of Rift Valley fever. Viruses 3:493–519
doi: 10.3390/v3050493 pubmed: 21666766 pmcid: 3111045
Indran SV, Ikegami T (2012) Novel approaches to develop Rift Valley fever vaccines. Front Cell Infect Microbiol. https://doi.org/10.3389/fcimb.2012.00131
doi: 10.3389/fcimb.2012.00131 pubmed: 23112960 pmcid: 3481114
Faburay B, LaBeaud AD, McVey DS, Wilson WC, Richt JA (2017) Current status of Rift Valley fever vaccine development. Vaccines. https://doi.org/10.3390/vaccines5030029
doi: 10.3390/vaccines5030029 pubmed: 28925970 pmcid: 5620560
Linthicum KJ, Britch SC, Anyamba A (2016) Rift Valley fever: an emerging mosquito-borne disease. Annu Rev Entomol 61:395–415
doi: 10.1146/annurev-ento-010715-023819 pubmed: 26982443
Lumley S et al (2017) Rift Valley fever virus: strategies for maintenance, survival and vertical transmission in mosquitoes. J Gen Virol 98:875–887
doi: 10.1099/jgv.0.000765 pubmed: 28555542
Olive MM, Goodman SM, Reynes JM (2012) The role of wild mammals in the maintenance of Rift Valley fever virus. J Wildl Dis 48:241–266
doi: 10.7589/0090-3558-48.2.241 pubmed: 22493102
Beechler BR et al (2015) Rift Valley fever in Kruger national park: do buffalo play a role in the inter-epidemic circulation of virus? Transbound Emerg Dis 62:24–32
doi: 10.1111/tbed.12197 pubmed: 24330522
Mroz C et al (2017) Seroprevalence of Rift Valley fever virus in livestock during inter-epidemic period in Egypt, 2014/15. BMC Vet Res. https://doi.org/10.1186/s12917-017-0993-8
doi: 10.1186/s12917-017-0993-8 pubmed: 28381251 pmcid: 5382484
Brustolin M et al (2017) Rift Valley fever virus and European mosquitoes: vector competence of Culex pipiens and Stegomyia albopicta (= Aedes albopictus). Med Vet Entomol 31:365–372
doi: 10.1111/mve.12254 pubmed: 28782121
Turell MJ, Wilson WC, Bennett KE (2010) Potential for North American mosquitoes (Diptera: Culicidae) to transmit rift Valley fever virus. J Med Entomol 47:884–889
doi: 10.1093/jmedent/47.5.884 pubmed: 20939385
Turell MJ et al (2015) Potential for Psorophora columbiae and Psorophora ciliata mosquitoes (Diptera: Culicidae) to transmit Rift Valley fever virus. J Med Entomol 52:1111–1116
doi: 10.1093/jme/tjv093 pubmed: 26336233
Gaudreault NN, Indran SV, Bryant PK, Richt JA, Wilson WC (2015) Comparison of Rift Valley fever virus replication in North American livestock and wildlife cell lines. Front Microbiol 6:664
doi: 10.3389/fmicb.2015.00664 pubmed: 26175725 pmcid: 4485352
Adams MJ et al (2017) Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2017). Arch Virol 162:2505–2538
doi: 10.1007/s00705-017-3358-5 pubmed: 28434098
Freiberg AN, Sherman MB, Morais MC, Holbrook MR, Watowich SJ (2008) Three-dimensional organization of Rift Valley fever virus revealed by cryoelectron tomography. J Virol 82:10341–10348
doi: 10.1128/JVI.01191-08 pubmed: 18715915 pmcid: 2573222
Ellis DS, Simpson DI, Stamford S, Abdel Wahab KS (1979) Rift Valley fever virus: some ultrastructural observations on material from the outbreak in Egypt 1977. J Gen Virol 42:329–337
doi: 10.1099/0022-1317-42-2-329 pubmed: 422955
Hornak KE, Lanchy JM, Lodmell JS (2016) RNA encapsidation and packaging in the phleboviruses. Viruses. https://doi.org/10.3390/v8070194
doi: 10.3390/v8070194 pubmed: 27428993 pmcid: 4974529
Huiskonen JT, Overby AK, Weber F, Grunewald K (2009) Electron cryo-microscopy and single-particle averaging of Rift Valley fever virus: evidence for GN-GC glycoprotein heterodimers. J Virol 83:3762–3769
doi: 10.1128/JVI.02483-08 pubmed: 19193794 pmcid: 2663282
Sherman MB, Freiberg AN, Holbrook MR, Watowich SJ (2009) Single-particle cryo-electron microscopy of Rift Valley fever virus. Virology 387:11–15
doi: 10.1016/j.virol.2009.02.038 pubmed: 19304307 pmcid: 2673237
Rusu M et al (2012) An assembly model of Rift Valley fever virus. Front Microbiol 3:254
doi: 10.3389/fmicb.2012.00254 pubmed: 22837754 pmcid: 3400131
Raymond DD, Piper ME, Gerrard SR, Smith JL (2010) Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation. Proc Natl Acad Sci USA 107:11769–11774
doi: 10.1073/pnas.1001760107 pubmed: 20547879
Kakach LT, Suzich JA, Collett MS (1989) Rift Valley fever virus M segment: phlebovirus expression strategy and protein glycosylation. Virology 170:505–510
doi: 10.1016/0042-6822(89)90442-X pubmed: 2728348
Wasmoen TL, Kakach LT, Collett MS (1988) Rift Valley fever virus M segment: cellular localization of M segment-encoded proteins. Virology 166:275–280
doi: 10.1016/0042-6822(88)90174-2 pubmed: 3046119
Suzich JA, Kakach LT, Collett MS (1990) Expression strategy of a phlebovirus: biogenesis of proteins from the Rift Valley fever virus M segment. J Virol 64:1549–1555
pubmed: 2319645 pmcid: 249289
Kakach LT, Wasmoen TL, Collett MS (1988) Rift Valley fever virus M segment: use of recombinant vaccinia viruses to study Phlebovirus gene expression. J Virol 62:826–833
pubmed: 3339714 pmcid: 253638
Kreher F et al (2014) The Rift Valley fever accessory proteins NSm and P78/NSm-G(N) are distinct determinants of virus propagation in vertebrate and invertebrate hosts. Emerg Microbes Infect 3(10):e71. https://doi.org/10.1038/emi.2014.71
Gauliard N, Billecocq A, Flick R, Bouloy M (2006) Rift Valley fever virus noncoding regions of L, M and S segments regulate RNA synthesis. Virology 351:170–179
doi: 10.1016/j.virol.2006.03.018 pubmed: 16630639
Piper ME, Sorenson DR, Gerrard SR (2011) Efficient cellular release of Rift Valley fever virus requires genomic RNA. PLoS ONE 6:e18070
doi: 10.1371/journal.pone.0018070 pubmed: 21445316 pmcid: 3061922
Habjan M et al (2009) NSs protein of Rift Valley fever virus induces the specific degradation of the double-stranded RNA-dependent protein kinase. J Virol 83:4365–4375
doi: 10.1128/JVI.02148-08 pubmed: 19211744 pmcid: 2668506
Ikegami T, Won S, Peters CJ, Makino S (2005) Rift Valley fever virus NSs mRNA is transcribed from an incoming anti-viral-sense S RNA segment. J Virol 79:12106–12111
doi: 10.1128/JVI.79.18.12106-12111.2005 pubmed: 16140788 pmcid: 1212623
Gerrard SR, Bird BH, Albarino CG, Nichol ST (2007) The NSm proteins of Rift Valley fever virus are dispensable for maturation, replication and infection. Virology 359:459–465
doi: 10.1016/j.virol.2006.09.035 pubmed: 17070883
Crabtree MB et al (2012) Infection and transmission of Rift Valley fever viruses lacking the NSs and/or NSm genes in mosquitoes: potential role for NSm in mosquito infection. PLoS Negl Trop Dis 6:e1639
doi: 10.1371/journal.pntd.0001639 pubmed: 22563517 pmcid: 3341344
Won SY, Ikegami T, Peters CJ, Makino S (2007) NSm protein of Rift Valley fever virus suppresses virus-induced apoptosis. J Virol 81:13335–13345
doi: 10.1128/JVI.01238-07 pubmed: 17913816 pmcid: 2168885
Terasaki K, Won S, Makino S (2013) The C-terminal region of Rift Valley fever virus NSm protein targets the protein to the mitochondrial outer membrane and exerts antiapoptotic function. J Virol 87:676–682
doi: 10.1128/JVI.02192-12 pubmed: 23097454 pmcid: 3536385
Lihoradova O, Ikegami T (2014) Countermeasure development for Rift Valley fever: deletion, modification or targeting of major virulence factor NSs. Future Virol 9:27–39
doi: 10.2217/fvl.13.117 pubmed: 24910709 pmcid: 4043376
Yadani FZ, Kohl A, Prehaud C, Billecocq A, Bouloy M (1999) The carboxy-terminal acidic domain of Rift Valley Fever virus NSs protein is essential for the formation of filamentous structures but not for the nuclear localization of the protein. J Virol 73:5018–5025
pubmed: 10233964 pmcid: 112546
Bouloy M et al (2001) Genetic evidence for an interferon-antagonistic function of Rift Valley fever virus nonstructural protein NSs. J Virol 75:1371–1377
doi: 10.1128/JVI.75.3.1371-1377.2001 pubmed: 11152510 pmcid: 114043
Le May N et al (2008) A SAP30 complex inhibits IFN-beta expression in Rift Valley fever virus infected cells. PLoS Pathog 4:e13
doi: 10.1371/journal.ppat.0040013 pubmed: 18225953 pmcid: 2323286
Dasgupta A (2004) Targeting TFIIH to inhibit host cell transcription by Rift Valley fever virus. Mol Cell 13:456–458
doi: 10.1016/S1097-2765(04)00092-9 pubmed: 14992716
Cyr N et al (2015) A OmegaXaV motif in the Rift Valley fever virus NSs protein is essential for degrading p62, forming nuclear filaments and virulence. Proc Natl Acad Sci USA 112:6021–6026
doi: 10.1073/pnas.1503688112 pubmed: 25918396
Kainulainen M et al (2014) Virulence factor NSs of Rift Valley fever virus recruits the F-box protein FBXO3 to degrade subunit p62 of general transcription factor TFIIH. J Virol 88:3464–3473
doi: 10.1128/JVI.02914-13 pubmed: 24403578 pmcid: 3957945
Kalveram B, Lihoradova O, Ikegami T (2011) NSs protein of Rift Valley fever virus promotes posttranslational downregulation of the TFIIH subunit p62. J Virol 85:6234–6243
doi: 10.1128/JVI.02255-10 pubmed: 21543505 pmcid: 3126510
Ikegami T et al (2009) Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2alpha phosphorylation. PLoS Pathog 5:e1000287
doi: 10.1371/journal.ppat.1000287 pubmed: 19197350 pmcid: 2629125
Dalet A, Gatti E, Pierre P (2015) Integration of PKR-dependent translation inhibition with innate immunity is required for a coordinated anti-viral response. FEBS Lett 589:1539–1545
doi: 10.1016/j.febslet.2015.05.006 pubmed: 25979169
Gale M Jr, Tan SL, Katze MG (2000) Translational control of viral gene expression in eukaryotes. Microbiol Mol Biol Rev 64:239–280
doi: 10.1128/MMBR.64.2.239-280.2000 pubmed: 10839817 pmcid: 98994
Kalveram B, Lihoradova O, Indran SV, Head JA, Ikegami T (2013) Using click chemistry to measure the effect of viral infection on host-cell RNA synthesis. J Vis Exp (78):e50809. https://doi.org/10.3791/50809
Mansuroglu Z et al (2010) Nonstructural NSs protein of Rift Valley fever virus interacts with pericentromeric DNA sequences of the host cell, inducing chromosome cohesion and segregation defects. J Virol 84:928–939
doi: 10.1128/JVI.01165-09 pubmed: 19889787
Copeland AM, Altamura LA, Van Deusen NM, Schmaljohn CS (2013) Nuclear relocalization of polyadenylate binding protein during Rift Valley fever virus infection involves expression of the NSs gene. J Virol 87:11659–11669
doi: 10.1128/JVI.01434-13 pubmed: 23966414 pmcid: 3807323
Copeland AM, Van Deusen NM, Schmaljohn CS (2015) Rift Valley fever virus NSs gene expression correlates with a defect in nuclear mRNA export. Virology 486:88–93
doi: 10.1016/j.virol.2015.09.003 pubmed: 26410240
Ly HJ, Ikegami T (2016) Rift Valley fever virus NSs protein functions and the similarity to other bunyavirus NSs proteins. Virol J 13:118
doi: 10.1186/s12985-016-0573-8 pubmed: 27368371 pmcid: 4930582
Austin D et al (2012) p53 Activation following Rift Valley fever virus infection contributes to cell death and viral production. PLoS ONE 7:e36327
doi: 10.1371/journal.pone.0036327 pubmed: 22574148 pmcid: 3344861
Baer A et al (2012) Induction of DNA damage signaling upon Rift Valley fever virus infection results in cell cycle arrest and increased viral replication. J Biol Chem 287:7399–7410
doi: 10.1074/jbc.M111.296608 pubmed: 22223653 pmcid: 3293538
Narayanan A et al (2014) Reactive oxygen species activate NFkappaB (p65) and p53 and induce apoptosis in RVFV infected liver cells. Virology 449:270–286
doi: 10.1016/j.virol.2013.11.023 pubmed: 24418562
Schreur PJW, Kortekaas J (2016) Single-molecule FISH reveals non-selective packaging of Rift Valley fever virus genome segments. PLoS Pathog 12:e1005800
doi: 10.1371/journal.ppat.1005800
Carnec X, Ermonval M, Kreher F, Flamand M, Bouloy M (2014) Role of the cytosolic tails of Rift Valley fever virus envelope glycoproteins in viral morphogenesis. Virology 448:1–14
doi: 10.1016/j.virol.2013.09.023 pubmed: 24314631
Gerrard SR, Rollin PE, Nichol ST (2002) Bidirectional infection and release of Rift Valley fever virus in polarized epithelial cells. Virology 301:226–235
doi: 10.1006/viro.2002.1588 pubmed: 12359425
Gerrard SR, Nichol ST (2002) Characterization of the Golgi retention motif of Rift Valley fever virus G(N) glycoprotein. J Virol 76:12200–12210
doi: 10.1128/JVI.76.23.12200-12210.2002 pubmed: 12414959 pmcid: 136907
Gerrard SR, Nichol ST (2007) Synthesis, proteolytic processing and complex formation of N-terminally nested precursor proteins of the Rift Valley fever virus glycoproteins. Virology 357:124–133
doi: 10.1016/j.virol.2006.08.002 pubmed: 16963099
Murakami S, Terasaki K, Narayanan K, Makino S (2012) Roles of the coding and noncoding regions of Rift Valley fever virus RNA genome segments in viral RNA packaging. J Virol 86:4034–4039
doi: 10.1128/JVI.06700-11 pubmed: 22278239 pmcid: 3302519
Terasaki K, Murakami S, Lokugamage KG, Makino S (2011) Mechanism of tripartite RNA genome packaging in Rift Valley fever virus. Proc Natl Acad Sci USA 108:804–809
doi: 10.1073/pnas.1013155108 pubmed: 21187405
Brennan B, Welch SR, McLees A, Elliott RM (2011) Creation of a recombinant Rift Valley fever virus with a two-segmented genome. J Virol 85:10310–10318
doi: 10.1128/JVI.05252-11 pubmed: 21795328 pmcid: 3196426
Brennan B, Welch SR, Elliott RM (2014) The consequences of reconfiguring the ambisense S genome segment of Rift Valley fever virus on viral replication in mammalian and mosquito cells and for genome packaging. PLoS Pathog 10:e1003922
doi: 10.1371/journal.ppat.1003922 pubmed: 24550727 pmcid: 3923772
Wichgers Schreur PJ, Oreshkova N, Moormann RJ, Kortekaas J (2014) Creation of Rift Valley fever viruses with four-segmented genomes reveals flexibility in bunyavirus genome packaging. J Virol 88:10883–10893
doi: 10.1128/JVI.00961-14 pubmed: 25008937 pmcid: 4178868
Ikegami T, Peters CJ, Makino S (2005) Rift Valley fever virus nonstructural protein NSs promotes viral RNA replication and transcription in a minigenome system. J Virol 79:5606–5615
doi: 10.1128/JVI.79.9.5606-5615.2005 pubmed: 15827175 pmcid: 1082746
Sall AA et al (1997) Variability of the NS(S) protein among Rift Valley fever virus isolates. J Gen Virol 78(Pt 11):2853–2858
doi: 10.1099/0022-1317-78-11-2853 pubmed: 9367372
Sall AA et al (1999) Genetic reassortment of Rift Valley fever virus in nature. J Virol 73:8196–8200
pubmed: 10482570 pmcid: 112837
Bird BH, Khristova ML, Rollin PE, Ksiazek TG, Nichol ST (2007) Complete genome analysis of 33 ecologically and biologically diverse Rift Valley fever virus strains reveals widespread virus movement and low genetic diversity due to recent common ancestry. J Virol 81:2805–2816
doi: 10.1128/JVI.02095-06 pubmed: 17192303
Liu J et al (2017) The first imported case of Rift Valley fever in China reveals a genetic reassortment of different viral lineages. Emerg Microbes Infect 6:e4
doi: 10.1038/emi.2016.136 pubmed: 28096531 pmcid: 5285499
Grobbelaar AA et al (2011) Molecular epidemiology of Rift Valley fever virus. Emerg Infect Dis 17:2270–2276
doi: 10.3201/eid1712.111035 pubmed: 22172568 pmcid: 3311189
Bird BH et al (2008) Multiple virus lineages sharing recent common ancestry were associated with a large Rift Valley fever outbreak among livestock in Kenya during 2006–2007. J Virol 82:11152–11166
doi: 10.1128/JVI.01519-08 pubmed: 18786992 pmcid: 2573244
Saluzzo JF, Smith JF (1990) Use of reassortant viruses to map attenuating and temperature-sensitive mutations of the Rift Valley fever virus MP-12 vaccine. Vaccine 8:369–375
doi: 10.1016/0264-410X(90)90096-5 pubmed: 2396475
Turell MJ, Saluzzo JF, Tammariello RF, Smith JF (1990) Generation and transmission of Rift Valley fever viral reassortants by the mosquito Culex pipiens. J Gen Virol 71(Pt 10):2307–2312
doi: 10.1099/0022-1317-71-10-2307 pubmed: 2230736
Meegan JM (1979) The Rift Valley fever epizootic in Egypt 1977-78. 1. Description of the epizootic and virological studies. Trans R Soc Trop Med Hyg 73:618–623
doi: 10.1016/0035-9203(79)90004-X pubmed: 538803
Saluzzo JF, Anderson GW Jr, Hodgson LA, Digoutte JP, Smith JF (1989) Antigenic and biological properties of Rift Valley fever virus isolated during the 1987 Mauritanian epidemic. Res Virol 140:155–164
doi: 10.1016/S0923-2516(89)80093-7 pubmed: 2474189
Caplen H, Peters CJ, Bishop DH (1985) Mutagen-directed attenuation of Rift Valley fever virus as a method for vaccine development. J Gen Virol 66(Pt 10):2271–2277
doi: 10.1099/0022-1317-66-10-2271 pubmed: 4045430
Ly HJ, Lokugamage N, Nishiyama S, Ikegami T (2017) Risk analysis of inter-species reassortment through a Rift Valley fever phlebovirus MP-12 vaccine strain. PLoS ONE 12:e0185194
doi: 10.1371/journal.pone.0185194 pubmed: 28926632 pmcid: 5604998
Freire CC et al (2015) Reassortment and distinct evolutionary dynamics of Rift Valley fever virus genomic segments. Sci Rep 5:11353
doi: 10.1038/srep11353 pubmed: 26100494 pmcid: 4477411
Gerrard SR, Li L, Barrett AD, Nichol ST (2004) Ngari virus is a Bunyamwera virus reassortant that can be associated with large outbreaks of hemorrhagic fever in Africa. J Virol 78:8922–8926
doi: 10.1128/JVI.78.16.8922-8926.2004 pubmed: 15280501 pmcid: 479050
Briese T, Bird B, Kapoor V, Nichol ST, Lipkin WI (2006) Batai and Ngari viruses: M segment reassortment and association with severe febrile disease outbreaks in East Africa. J Virol 80:5627–5630
doi: 10.1128/JVI.02448-05 pubmed: 16699043 pmcid: 1472162
Vialat P, Muller R, Vu TH, Prehaud C, Bouloy M (1997) Mapping of the mutations present in the genome of the Rift Valley fever virus attenuated MP12 strain and their putative role in attenuation. Virus Res 52:43–50
doi: 10.1016/S0168-1702(97)00097-X pubmed: 9453143
Ikegami T et al (2015) Rift Valley fever virus MP-12 vaccine is fully attenuated by a combination of partial attenuations in the S, M, and L segments. J Virol 89:7262–7276
doi: 10.1128/JVI.00135-15 pubmed: 25948740 pmcid: 4473576
Lokugamage N, Ikegami T (2017) Genetic stability of Rift Valley fever virus MP-12 vaccine during serial passages in culture cells. NPJ Vaccines 2. https://doi.org/10.1038/s41541-017-0021-9
Eiden M et al (2014) Ngari virus in goats during Rift Valley fever outbreak, Mauritania, 2010. Emerg Infect Dis 20:2174–2176
doi: 10.3201/eid2012.140787 pubmed: 25419696 pmcid: 4257808
Bowen MD et al (2001) A reassortant bunyavirus isolated from acute hemorrhagic fever cases in Kenya and Somalia. Virology 291:185–190
doi: 10.1006/viro.2001.1201 pubmed: 11878887

Auteurs

Natasha N Gaudreault (NN)

Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, 1800 Denison Avenue, Manhattan, KS, 66506, USA. nng5757@vet.k-state.edu.

Sabarish V Indran (SV)

Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, 1800 Denison Avenue, Manhattan, KS, 66506, USA.

Velmurugan Balaraman (V)

Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, 1800 Denison Avenue, Manhattan, KS, 66506, USA.

William C Wilson (WC)

United States Department of Agriculture, Agricultural Research Service, Arthropod Borne Animal Disease Research Unit, 1515 College Avenue, Manhattan, KS, 66506, USA.

Juergen A Richt (JA)

Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, 1800 Denison Avenue, Manhattan, KS, 66506, USA. jricht@ksu.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH