Impact of sex on outcomes after surgery for non-muscle-invasive and muscle-invasive bladder urothelial carcinoma: a systematic review and meta-analysis
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu metaanalýza, systematický přehled, časopisecké články
PubMed
35963957
PubMed Central
PMC10159976
DOI
10.1007/s00345-022-04116-x
PII: 10.1007/s00345-022-04116-x
Knihovny.cz E-zdroje
- Klíčová slova
- Meta-analysis, Muscle-invasive bladder urothelial carcinoma, Non-muscle-invasive bladder urothelial carcinoma, Sex,
- MeSH
- karcinom z přechodných buněk * patologie MeSH
- lidé MeSH
- močový měchýř patologie MeSH
- nádory močového měchýře * patologie MeSH
- prognóza MeSH
- proporcionální rizikové modely MeSH
- Check Tag
- lidé MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- metaanalýza MeSH
- systematický přehled MeSH
PURPOSE: To assess the prognostic value of sex for non-muscle-invasive/muscle-invasive bladder urothelial carcinoma (NMIBC/MIBC) treated with radical surgery. METHODS: The PubMed, Web of Science, and Scopus databases were searched in November 2021 according to the Preferred Reporting Items for Systematic Review and Meta-analysis statement. Studies were deemed eligible if they involved the comparison of the overall, cancer-specific, progression, and recurrence-free survival of patients with NMIBC/MIBC. Formal sex-stratified meta-analyses of these outcomes were performed. RESULTS: Thirty-one studies, which included 32,525 patients with NMIBC, and 63 studies, which included 85,132 patients with MIBC, were eligible for review and meta-analysis. Female sex was associated with worse cancer-specific survival (pooled hazard ratio [HR], 1.21; 95% confidence interval [CI], 1.11-1.31) and overall survival (pooled HR, 1.02; 95% CI, 1.00-1.05) in patients with MIBC. In contrast, however, sex was not associated with cancer-specific survival (pooled HR, 1.01; 95% CI, 0.70-1.46), progression-free survival (pooled HR, 1.04; 95% CI, 0.88-1.24), and recurrence-free survival (pooled HR, 1.06; 95% CI, 0.98-1.16) in patients with NMIBC. CONCLUSIONS: Sex is associated with an increased risk of worse survival outcomes in patients with MIBC but not in those with NMIBC. Given the genetic and social differences between sexes, sex may represent a key factor in the clinical decision-making process.
Department of Surgery S H Ho Urology Centre The Chinese University of Hong Kong Hong Kong China
Department of Urology 2nd Faculty of Medicine Charles University Prague Czech Republic
Department of Urology Comprehensive Cancer Center Medical University of Vienna Vienna Austria
Department of Urology King Fahad Specialist Hospital Dammam Saudi Arabia
Department of Urology Medical University of Silesia Zabrze Poland
Department of Urology San Raffaele Hospital Milan Italy
Department of Urology The Jikei University School of Medicine Tokyo Japan
Department of Urology University of Texas Southwestern Dallas TX USA
Department of Urology Weill Cornell Medical College New York NY USA
Division of Urology Department of Special Surgery The University of Jordan Amman Jordan
Division of Urology Department of Surgical Sciences University of Studies of Torino Turin Italy
Institute for Urology and Reproductive Health Sechenov University Moscow Russia
Karl Landsteiner Institute of Urology and Andrology Vienna Austria
Research Center for Evidence Based Medicine Tabriz University of Medical Sciences Tabriz Iran
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Babjuk M, Burger M, Capoun O, Cohen D, Compérat EM, Dominguez Escrig JL, Gontero P, Liedberg F, Masson-Lecomte A, Mostafid AH, Palou J, van Rhijn BWG, Rouprêt M, Shariat SF, Seisen T, Soukup V, Sylvester RJ. European association of urology guidelines on non-muscle-invasive bladder cancer (Ta, T1, and carcinoma in Situ) Eur Urol. 2022;81(1):75–94. doi: 10.1016/j.eururo.2021.08.010. PubMed DOI
Mori K, D'Andrea D, Enikeev DV, Egawa S, Shariat SF. En bloc resection for nonmuscle invasive bladder cancer: review of the recent literature. Curr Opin Urol. 2020;30(1):41–47. doi: 10.1097/mou.0000000000000697. PubMed DOI
Mori K, Miura N, Babjuk M, Karakiewicz PI, Mostafaei H, Laukhtina E, Quhal F, Motlagh RS, Pradere B, Kimura S, Egawa S, Shariat SF. Low compliance to guidelines in nonmuscle-invasive bladder carcinoma: a systematic review. Urol Oncol. 2020;38(10):774–782. doi: 10.1016/j.urolonc.2020.06.013. PubMed DOI
Wallerand H, Bernhard JC, Culine S, Ballanger P, Robert G, Reiter RE, Ferrière JM, Ravaud A. Targeted therapies in non-muscle-invasive bladder cancer according to the signaling pathways. Urol Oncol. 2011;29(1):4–11. doi: 10.1016/j.urolonc.2009.07.025. PubMed DOI
Burger M, Catto JW, Dalbagni G, Grossman HB, Herr H, Karakiewicz P, Kassouf W, Kiemeney LA, La Vecchia C, Shariat S, Lotan Y. Epidemiology and risk factors of urothelial bladder cancer. Eur Urol. 2013;63(2):234–241. doi: 10.1016/j.eururo.2012.07.033. PubMed DOI
Shariat SF, Karakiewicz PI, Palapattu GS, Lotan Y, Rogers CG, Amiel GE, Vazina A, Gupta A, Bastian PJ, Sagalowsky AI, Schoenberg MP, Lerner SP. Outcomes of radical cystectomy for transitional cell carcinoma of the bladder: a contemporary series from the bladder cancer research consortium. J Urol. 2006;176(6 Pt 1):2414–2422. doi: 10.1016/j.juro.2006.08.004. PubMed DOI
Xylinas E, Kent M, Kluth L, Pycha A, Comploj E, Svatek RS, Lotan Y, Trinh QD, Karakiewicz PI, Holmang S, Scherr DS, Zerbib M, Vickers AJ, Shariat SF. Accuracy of the EORTC risk tables and of the CUETO scoring model to predict outcomes in non-muscle-invasive urothelial carcinoma of the bladder. Br J Cancer. 2013;109(6):1460–1466. doi: 10.1038/bjc.2013.372. PubMed DOI PMC
Witjes JA, Bruins HM, Cathomas R, Compérat EM, Cowan NC, Gakis G, Hernández V, Linares Espinós E, Lorch A, Neuzillet Y, Rouanne M, Thalmann GN, Veskimäe E, Ribal MJ, van der Heijden AG. European association of urology guidelines on muscle-invasive and metastatic bladder cancer: summary of the 2020 guidelines. Eur Urol. 2021;79(1):82–104. doi: 10.1016/j.eururo.2020.03.055. PubMed DOI
Abdollah F, Gandaglia G, Thuret R, Schmitges J, Tian Z, Jeldres C, Passoni NM, Briganti A, Shariat SF, Perrotte P, Montorsi F, Karakiewicz PI, Sun M. Incidence, survival and mortality rates of stage-specific bladder cancer in United States: a trend analysis. Cancer Epidemiol. 2013;37(3):219–225. doi: 10.1016/j.canep.2013.02.002. PubMed DOI
Zargar H, Espiritu PN, Fairey AS, Mertens LS, Dinney CP, Mir MC, Krabbe LM, Cookson MS, Jacobsen NE, Gandhi NM, Griffin J, Montgomery JS, Vasdev N, Yu EY, Youssef D, Xylinas E, Campain NJ, Kassouf W, Dall'Era MA, Seah JA, Ercole CE, Horenblas S, Sridhar SS, McGrath JS, Aning J, Shariat SF, Wright JL, Thorpe AC, Morgan TM, Holzbeierlein JM, Bivalacqua TJ, North S, Barocas DA, Lotan Y, Garcia JA, Stephenson AJ, Shah JB, van Rhijn BW, Daneshmand S, Spiess PE, Black PC. Multicenter assessment of neoadjuvant chemotherapy for muscle-invasive bladder cancer. Eur Urol. 2015;67(2):241–249. doi: 10.1016/j.eururo.2014.09.007. PubMed DOI PMC
Kluth LA, Black PC, Bochner BH, Catto J, Lerner SP, Stenzl A, Sylvester R, Vickers AJ, Xylinas E, Shariat SF. Prognostic and prediction tools in bladder cancer: a comprehensive review of the literature. Eur Urol. 2015;68(2):238–253. doi: 10.1016/j.eururo.2015.01.032. PubMed DOI
Putluri N, Shojaie A, Vasu VT, Vareed SK, Nalluri S, Putluri V, Thangjam GS, Panzitt K, Tallman CT, Butler C, Sana TR, Fischer SM, Sica G, Brat DJ, Shi H, Palapattu GS, Lotan Y, Weizer AZ, Terris MK, Shariat SF, Michailidis G, Sreekumar A. Metabolomic profiling reveals potential markers and bioprocesses altered in bladder cancer progression. Can Res. 2011;71(24):7376–7386. doi: 10.1158/0008-5472.can-11-1154. PubMed DOI PMC
Mori K, Abufaraj M, Mostafaei H, Quhal F, Karakiewicz PI, Briganti A, Kimura S, Egawa S, Shariat SF. A systematic review and meta-analysis of variant histology in urothelial carcinoma of the bladder treated with radical cystectomy. J Urol. 2020;204(6):1129–1140. doi: 10.1097/ju.0000000000001305. PubMed DOI
Mori K, Mostafaei H, Enikeev DV, Lysenko I, Quhal F, Kimura S, Karakiewicz PI, Egawa S, Shariat SF. Differential effect of sex on outcomes after radical surgery for upper tract and bladder urothelial carcinoma: a systematic review and meta-analysis. J Urol. 2020;204(1):58–62. doi: 10.1097/ju.0000000000000788. PubMed DOI
Mori K, Miura N, Mostafaei H, Quhal F, Motlagh RS, Lysenko I, Kimura S, Egawa S, Karakiewicz PI, Shariat SF. Prognostic value of preoperative hematologic biomarkers in urothelial carcinoma of the bladder treated with radical cystectomy: a systematic review and meta-analysis. Int J Clin Oncol. 2020;25(8):1459–1474. doi: 10.1007/s10147-020-01690-1. PubMed DOI PMC
Mori K, Schuettfort VM, Katayama S, Laukhtina E, Pradere B, Quhal F, Sari Motlagh R, Mostafaei H, Grossmann NC, Rajwa P, König F, Aydh A, Soria F, Moschini M, Karakiewicz PI, Lotan Y, Scherr D, Haydter M, Nyirady P, Teoh JYC, Egawa S, Compérat E, Shariat SF. The value of preoperative plasma VEGF levels in urothelial carcinoma of the bladder treated with radical cystectomy. Eur Urol Focus. 2021 doi: 10.1016/j.euf.2021.08.006. PubMed DOI
Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA: Cancer J Clin. 2022;72(1):7–33. doi: 10.3322/caac.21708. PubMed DOI
Lucca I, Klatte T, Fajkovic H, de Martino M, Shariat SF. Gender differences in incidence and outcomes of urothelial and kidney cancer. Nat Rev Urol. 2015;12(10):585–592. doi: 10.1038/nrurol.2015.232. PubMed DOI
Dobruch J, Daneshmand S, Fisch M, Lotan Y, Noon AP, Resnick MJ, Shariat SF, Zlotta AR, Boorjian SA. Gender and bladder cancer: a collaborative review of etiology, biology, and outcomes. Eur Urol. 2016;69(2):300–310. doi: 10.1016/j.eururo.2015.08.037. PubMed DOI
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hróbjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S, McGuinness LA, Stewart LA, Thomas J, Tricco AC, Welch VA, Whiting P, Moher D. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ (Clin Res Ed) 2021;372:n71. doi: 10.1136/bmj.n71. PubMed DOI PMC
Altman DG, Bland JM. How to obtain the P value from a confidence interval. BMJ. 2011;343:d2304. doi: 10.1136/bmj.d2304. PubMed DOI
Altman DG, Bland JM. How to obtain the confidence interval from a P value. BMJ. 2011;343:d2090. doi: 10.1136/bmj.d2090. PubMed DOI
DerSimonian R, Kacker R. Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials. 2007;28(2):105–114. doi: 10.1016/j.cct.2006.04.004. PubMed DOI
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–188. doi: 10.1016/0197-2456(86)90046-2. PubMed DOI
Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–560. doi: 10.1136/bmj.327.7414.557. PubMed DOI PMC
Scosyrev E, Noyes K, Feng C, Messing E. Sex and racial differences in bladder cancer presentation and mortality in the US. Cancer. 2009;115(1):68–74. doi: 10.1002/cncr.23986. PubMed DOI
Nielsen ME, Shariat SF, Karakiewicz PI, Lotan Y, Rogers CG, Amiel GE, Bastian PJ, Vazina A, Gupta A, Lerner SP, Sagalowsky AI, Schoenberg MP, Palapattu GS. Advanced age is associated with poorer bladder cancer-specific survival in patients treated with radical cystectomy. Eur Urol. 2007;51(3):699–706. doi: 10.1016/j.eururo.2006.11.004. PubMed DOI
Otto W, May M, Fritsche HM, Dragun D, Aziz A, Gierth M, Trojan L, Herrmann E, Moritz R, Ellinger J, Tilki D, Buchner A, Höfner T, Brookman-May S, Nuhn P, Gilfrich C, Roigas J, Zacharias M, Denzinger S, Hohenfellner M, Haferkamp A, Müller SC, Kocot A, Riedmiller H, Wieland WF, Stief CG, Bastian PJ, Burger M. Analysis of sex differences in cancer-specific survival and perioperative mortality following radical cystectomy: results of a large German multicenter study of nearly 2500 patients with urothelial carcinoma of the bladder. Gend Med. 2012;9(6):481–489. doi: 10.1016/j.genm.2012.11.001. PubMed DOI
Mansson A, Anderson H, Colleen S. Time lag to diagnosis of bladder cancer–influence of psychosocial parameters and level of health-care provision. Scand J Urol Nephrol. 1993;27(3):363–369. doi: 10.3109/00365599309180448. PubMed DOI
Hollenbeck BK, Dunn RL, Ye Z, Hollingsworth JM, Skolarus TA, Kim SP, Montie JE, Lee CT, Wood DP, Jr, Miller DC. Delays in diagnosis and bladder cancer mortality. Cancer. 2010;116(22):5235–5242. doi: 10.1002/cncr.25310. PubMed DOI
Davis R, Jones JS, Barocas DA, Castle EP, Lang EK, Leveillee RJ, Messing EM, Miller SD, Peterson AC, Turk TM, Weitzel W. Diagnosis, evaluation and follow-up of asymptomatic microhematuria (AMH) in adults: AUA guideline. J Urol. 2012;188(6 Suppl):2473–2481. doi: 10.1016/j.juro.2012.09.078. PubMed DOI
Bergman J, Neuhausen K, Chamie K, Scales CD, Carter S, Kwan L, Lerman SE, Aronson W, Litwin MS. Building a medical neighborhood in the safety net: an innovative technology improves hematuria workups. Urology. 2013;82(6):1277–1282. doi: 10.1016/j.urology.2013.08.015. PubMed DOI
Saez S, Martin PM. Evidence of estrogen receptors in the trigone area of human urinary bladder. J Steroid Biochem. 1981;15:317–320. doi: 10.1016/0022-4731(81)90291-0. PubMed DOI
Schilling D, Horstmann M, Nagele U, Sievert KD, Stenzl A. Cystectomy in women. BJU Int. 2008;102(9 Pt B):1289–1295. doi: 10.1111/j.1464-410X.2008.07972.x. PubMed DOI
Madeb R, Messing EM. Gender, racial and age differences in bladder cancer incidence and mortality. Urol Oncol. 2004;22(2):86–92. doi: 10.1016/s1078-1439(03)00139-x. PubMed DOI
Zhang Y. Understanding the gender disparity in bladder cancer risk: the impact of sex hormones and liver on bladder susceptibility to carcinogens. J Environ Sci Health, Part C Environ Carcinog Ecotoxicol Rev. 2013;31(4):287–304. doi: 10.1080/10590501.2013.844755. PubMed DOI PMC
Bolenz C, Lotan Y, Ashfaq R, Shariat SF. Estrogen and progesterone hormonal receptor expression in urothelial carcinoma of the bladder. Eur Urol. 2009;56(6):1093–1095. doi: 10.1016/j.eururo.2009.06.032. PubMed DOI
Boorjian S, Ugras S, Mongan NP, Gudas LJ, You X, Tickoo SK, Scherr DS. Androgen receptor expression is inversely correlated with pathologic tumor stage in bladder cancer. Urology. 2004;64(2):383–388. doi: 10.1016/j.urology.2004.03.025. PubMed DOI
Lombard AP, Mudryj M. The emerging role of the androgen receptor in bladder cancer. Endocr Relat Cancer. 2015;22(5):R265–277. doi: 10.1530/erc-15-0209. PubMed DOI
Gakis G, Stenzl A. Gender-specific differences in muscle-invasive bladder cancer: the concept of sex steroid sensitivity. World J Urol. 2013;31(5):1059–1064. doi: 10.1007/s00345-013-1037-z. PubMed DOI
Jing Y, Cui D, Guo W, Jiang J, Jiang B, Lu Y, Zhao W, Wang X, Jiang Q, Han B, Xia S. Activated androgen receptor promotes bladder cancer metastasis via Slug mediated epithelial-mesenchymal transition. Cancer Lett. 2014;348(1–2):135–145. doi: 10.1016/j.canlet.2014.03.018. PubMed DOI
Özdemir BC, Dotto GP. Sex hormones and anticancer immunity. Clin Cancer Res: Off J Am Assoc Cancer Res. 2019;25(15):4603–4610. doi: 10.1158/1078-0432.ccr-19-0137. PubMed DOI
McGrath M, Michaud DS, De Vivo I. Hormonal and reproductive factors and the risk of bladder cancer in women. Am J Epidemiol. 2006;163(3):236–244. doi: 10.1093/aje/kwj028. PubMed DOI
Daugherty SE, Lacey JV, Jr, Pfeiffer RM, Park Y, Hoover RN, Silverman DT. Reproductive factors and menopausal hormone therapy and bladder cancer risk in the NIH-AARP diet and health study. Int J Cancer. 2013;133(2):462–472. doi: 10.1002/ijc.28022. PubMed DOI PMC
Cantwell MM, Lacey JV, Jr, Schairer C, Schatzkin A, Michaud DS. Reproductive factors, exogenous hormone use and bladder cancer risk in a prospective study. Int J Cancer. 2006;119(10):2398–2401. doi: 10.1002/ijc.22175. PubMed DOI
Abelson B, Sun D, Que L, Nebel RA, Baker D, Popiel P, Amundsen CL, Chai T, Close C, DiSanto M, Fraser MO, Kielb SJ, Kuchel G, Mueller ER, Palmer MH, Parker-Autry C, Wolfe AJ, Damaser MS. Sex differences in lower urinary tract biology and physiology. Biol Sex Differ. 2018;9(1):45. doi: 10.1186/s13293-018-0204-8. PubMed DOI PMC
Webb K, Peckham H, Radziszewska A, Menon M, Oliveri P, Simpson F, Deakin CT, Lee S, Ciurtin C, Butler G, Wedderburn LR, Ioannou Y. Sex and Pubertal Differences in the type 1 interferon pathway associate with both X chromosome number and serum sex hormone concentration. Front Immunol. 2018;9:3167. doi: 10.3389/fimmu.2018.03167. PubMed DOI PMC
Koti M, Ingersoll MA, Gupta S, Lam CM, Li X, Kamat AM, Black PC, Siemens DR. Sex differences in bladder cancer immunobiology and outcomes: a collaborative review with implications for treatment. Eur Urol Oncol. 2020;3(5):622–630. doi: 10.1016/j.euo.2020.08.013. PubMed DOI
Shang Z, Li Y, Hsu I, Zhang M, Tian J, Wen S, Han R, Messing EM, Chang C, Niu Y, Yeh S. Targeting estrogen/estrogen receptor alpha enhances Bacillus Calmette-Guérin efficacy in bladder cancer. Oncotarget. 2016;7(19):27325–27335. doi: 10.18632/oncotarget.8756. PubMed DOI PMC
Zhang GJ, Crist SA, McKerrow AK, Xu Y, Ladehoff DC, See WA. Autocrine IL-6 production by human transitional carcinoma cells upregulates expression of the alpha5beta1 firbonectin receptor. J Urol. 2000;163(5):1553–1559. doi: 10.1016/S0022-5347(05)67678-1. PubMed DOI
Guise AI, Chen F, Zhang G, See W. The effects of physiological estrogen concentration on the immune response of urothelial carcinoma cells to bacillus Calmette-Guérin. J Urol. 2011;185(1):298–304. doi: 10.1016/j.juro.2010.09.004. PubMed DOI
Kavoussi LR, Brown EJ, Ritchey JK, Ratliff TL. Fibronectin-mediated Calmette-Guerin bacillus attachment to murine bladder mucosa requirement for the expression of an antitumor response. J Clin Investig. 1990;85(1):62–67. doi: 10.1172/jci114434. PubMed DOI PMC
Wang PF, Song HF, Zhang Q, Yan CX. Pan-cancer immunogenomic analyses reveal sex disparity in the efficacy of cancer immunotherapy. Eur J Cancer (Oxf, Engl) 2020;126:136–138. doi: 10.1016/j.ejca.2019.12.008. PubMed DOI
Conforti F, Pala L, Bagnardi V, De Pas T, Martinetti M, Viale G, Gelber RD, Goldhirsch A. Cancer immunotherapy efficacy and patients' sex: a systematic review and meta-analysis. Lancet Oncol. 2018;19(6):737–746. doi: 10.1016/s1470-2045(18)30261-4. PubMed DOI
Carè A, Bellenghi M, Matarrese P, Gabriele L, Salvioli S, Malorni W. Sex disparity in cancer: roles of microRNAs and related functional players. Cell Death Differ. 2018;25(3):477–485. doi: 10.1038/s41418-017-0051-x. PubMed DOI PMC
Mori K, Mostafaei H, Abufaraj M, Yang L, Egawa S, Shariat SF. Smoking and bladder cancer: review of the recent literature. Curr Opin Urol. 2020;30(5):720–725. doi: 10.1097/mou.0000000000000804. PubMed DOI
Rink M, Zabor EC, Furberg H, Xylinas E, Ehdaie B, Novara G, Babjuk M, Pycha A, Lotan Y, Trinh QD, Chun FK, Lee RK, Karakiewicz PI, Fisch M, Robinson BD, Scherr DS, Shariat SF. Impact of smoking and smoking cessation on outcomes in bladder cancer patients treated with radical cystectomy. Eur Urol. 2013;64(3):456–464. doi: 10.1016/j.eururo.2012.11.039. PubMed DOI
Freedman ND, Silverman DT, Hollenbeck AR, Schatzkin A, Abnet CC. Association between smoking and risk of bladder cancer among men and women. JAMA. 2011;306(7):737–745. doi: 10.1001/jama.2011.1142. PubMed DOI PMC
Rink M, Xylinas E, Trinh QD, Lotan Y, Margulis V, Raman JD, Fisch M, Lee RK, Chun FK, Abdennabi J, Seitz C, Pycha A, Zlotta AR, Karakiewicz PI, Babjuk M, Scherr DS, Shariat SF. Gender-specific effect of smoking on upper tract urothelial carcinoma outcomes. BJU Int. 2013;112(5):623–637. doi: 10.1111/bju.12014. PubMed DOI
Bi H, Tian Y, Song C, Li J, Liu T, Chen Z, Chen C, Huang Y, Zhang Y. Urinary microbiota - a potential biomarker and therapeutic target for bladder cancer. J Med Microbiol. 2019;68(10):1471–1478. doi: 10.1099/jmm.0.001058. PubMed DOI