Skip to main content

Advertisement

SpringerLink
Log in

Prevalence and Impact of Frailty in Pancreatic Cancer: A Systematic Review and Meta-Analysis Based on 35,191 Patients

  • Pancreatic Tumors
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Frailty has been associated with increased mortality among patients with pancreatic cancer. Nevertheless, several lines of evidence regarding the prevalence of frailty in patients with pancreatic cancer and mortality in patients with pancreatic cancer and frailty have not been thoroughly investigated and require clarification.

Methods

A systematic review and meta-analysis of studies indexed in PubMed, Scopus, Web of Science, and Embase through March 2023 were conducted, and the pooled prevalence and relative risk (RR) estimate were calculated.

Results

A total of 18 studies containing 35,191 patients with pancreatic cancer were included. The prevalence of frailty in pancreatic cancer was 45% (95% CI = 29–62; I2 = 99.9%; p = 0.000). In patients with pancreatic cancer, frailty was associated with increased relative risk for mortality (RR = 1.70; 95% CI = 1.30–2.22; I2 = 84.8%, p = 0.000).

Conclusions

Frailty prevalence in pancreatic cancer is common and exerts a significant negative impact on the survival of patients with pancreatic cancer. Our findings are characterized by significant heterogeneity, and caution is warranted in their interpretation. However, these findings highlight the importance of evaluating frailty, which may provide prognostic data and inform decision-making priorities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–249.

    Article  PubMed  Google Scholar 

  2. Huang J, Lok V, Ngai CH, et al. Worldwide burden of, risk factors for, and trends in pancreatic cancer. Gastroenterology. 2021;160(3):744–754.

    Article  PubMed  Google Scholar 

  3. Vincent A, Herman J, Schulick R, Hruban RH, Goggins M. Pancreatic cancer. Lancet. 2011;378(9791):607–620.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Klein AP. Pancreatic cancer epidemiology: understanding the role of lifestyle and inherited risk factors. Nat Rev Gastroenterol Hepatol. 2021;18(7):493–502.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Clegg A, Young J, Iliffe S, Rikkert MO, Rockwood K. Frailty in elderly people. Lancet. 2013;381(9868):752–762.

    Article  PubMed  Google Scholar 

  6. Fried LP, Tangen CM, Walston J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146-156.

    Article  CAS  PubMed  Google Scholar 

  7. Komici K, Cappuccio M, Scacchi A, et al. The prevalence and the impact of frailty in hepato-biliary pancreatic cancers: A systematic review and meta-analysis. J Clin Med. 2022;11(4).

  8. Veronese N, Custodero C, Cella A, et al. Prevalence of multidimensional frailty and pre-frailty in older people in different settings: a systematic review and meta-analysis. Ageing Res Rev. 2021;72:101498.

    Article  PubMed  Google Scholar 

  9. Houghton JSM, Nickinson ATO, Morton AJ, et al. Frailty factors and outcomes in vascular surgery patients: a systematic review and meta-analysis. Ann Surg. 2020;272(2):266–276.

    Article  PubMed  Google Scholar 

  10. Kochar A, Deo SV, Charest B, et al. Preoperative frailty and adverse outcomes following coronary artery bypass grafting surgery in US veterans. J Am Geriatr Soc. 2023;71(9):2736–2747.

    Article  PubMed  Google Scholar 

  11. Hewitt J, Long S, Carter B, Bach S, McCarthy K, Clegg A. The prevalence of frailty and its association with clinical outcomes in general surgery: a systematic review and meta-analysis. Age Ageing. 2018;47(6):793–800.

    Article  PubMed  Google Scholar 

  12. Augustin T, Burstein MD, Schneider EB, et al. Frailty predicts risk of life-threatening complications and mortality after pancreatic resections. Surgery. 2016;160(4):987–996.

    Article  PubMed  Google Scholar 

  13. Rostoft S, van Leeuwen B. Frailty assessment tools and geriatric assessment in older patients with hepatobiliary and pancreatic malignancies. Eur J Surg Oncol. 2021;47(3 Pt A):514–518.

  14. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. PLos Med. 2009;339:b2700.

    Google Scholar 

  15. von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: Guidelines for reporting observational studies. J Clin Epidemiol. 2014;12(12):1495–1499.

    Google Scholar 

  16. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–605.

    Article  PubMed  Google Scholar 

  17. Schmidt FL, Oh IS, Hayes TL. Fixed- versus random-effects models in meta-analysis: model properties and an empirical comparison of differences in results. Br J Math Stat Psychol. 2009;62(Pt 1):97–128.

    Article  PubMed  Google Scholar 

  18. Benjamin AJ, Buschmann MM, Schneider A, et al. Can comprehensive imaging analysis with analytic morphomics and geriatric assessment predict serious complications in patients undergoing pancreatic surgery? J Gastrointest Sur. 2017;21(6):1009–1016.

    Article  Google Scholar 

  19. Mogal H, Vermilion SA, Dodson R, et al. Modified frailty index predicts morbidity and mortality after pancreaticoduodenectomy. Ann Surg Oncol. 2017;24(6):1714–1721.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Ngo-Huang A, Holmes HM, des Bordes JKA, et al. Association between frailty syndrome and survival in patients with pancreatic adenocarcinoma. Cancer Med. 2019;8(6): 2867–2876.

  21. Nakano Y, Hirata Y, Shimogawara T, et al. Frailty is a useful predictive marker of postoperative complications after pancreaticoduodenectomy. World J Surg Oncol. 2020;18(1):194.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Al Abbas AI, Borrebach JD, Pitt HA, et al. Development of a novel pancreatoduodenectomy-specific risk calculator: An analysis of 10,000 patients. J Gastrointest Surg. 2021;25(6):1503–1511.

    Article  PubMed  Google Scholar 

  23. Gebbia V, Mare M, Cordio S, et al. Is G8 geriatric assessment tool useful in managing elderly patients with metastatic pancreatic carcinoma? J Geriatr Oncol. 2021;12(1):163–167.

    Article  CAS  PubMed  Google Scholar 

  24. Mima K, Hayashi H, Nakagawa S, et al. Frailty is associated with poor prognosis after resection for pancreatic cancer. Int J Clin Oncol. 2021;26(10):1938–1946.

    Article  PubMed  Google Scholar 

  25. Rieser CJ, Zenati M, Narayanan S, et al. Optimal management of resectable pancreatic head cancer in the elderly patient: does neoadjuvant therapy offer a survival benefit? Ann Surg Oncol. 2021;28(11):6264–6272.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Rittberg R, Zhang H, Lambert P, Kudlovich R, Kim CA, Dawe DE. Utility of the modified frailty index in predicting toxicity and cancer outcomes for older adults with advanced pancreatic cancer receiving first-line palliative chemotherapy. J Geriatr Oncol. 2021;12(1):112–117.

    Article  CAS  PubMed  Google Scholar 

  27. Yamada S, Shimada M, Morine Y, et al. Significance of frailty in prognosis after surgery in patients with pancreatic ductal adenocarcinoma. World J Surg Oncol. 2021;19(1):94.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Kadokura M, Mori Y, Takenaka Y, et al. Usefulness of the G8 geriatric assessment tool as a prognostic factor in gemcitabine plus nab-paclitaxel combination therapy for elderly patients with pancreatic cancer. JMA J. 2022;5(4):512–519.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kobayashi S, Suzuki M, Ueno M, et al. Comparing the efficacy and safety of gemcitabine plus nab-paclitaxel versus gemcitabine alone in older adults with unresectable pancreatic cancer. Oncologist. 2022;27(10):e774–e782.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Li V, Awan A, Serrano PE. Frailty predicts postoperative complications following pancreaticoduodenectomy. Eur Surg Res. 2022;63(4):232–240.

    Article  CAS  PubMed  Google Scholar 

  31. Lund CM, Mikkelsen MK, Theile S, et al. Age-related differences in recall of information and handling of chemotherapy-related side effects in cancer patients: the recap study. Oncologist. 2022;27(2):e185–e193.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Negrete-Najar JP, Sehovic M, Rodriquenz MG, Garcia-Martinez J, Extermann M. Development of a health data derived frailty index as a predictor of adverse outcomes in older patients with pancreatic cancer. J Geriatr Oncol. 2022;13(3):308–314.

    Article  CAS  PubMed  Google Scholar 

  33. Paiella S, De Pastena M, Esposito A, et al. Modified frailty index to assess risk in elderly patients undergoing distal pancreatectomy: a retrospective single-center study. World J Surg. 2022;46(4):891–900.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Scholer AJ, Marcus R, Garland-Kledzik M, et al. Validating biologic age in selecting elderly patients with pancreatic cancer for surgical resection. J Surg Oncol. 2023;127(3):394–404.

    Article  PubMed  Google Scholar 

  35. Dent E, Martin FC, Bergman H, Woo J, Romero-Ortuno R, Walston JD. Management of frailty: opportunities, challenges, and future directions. Lancet. 2019;394(10206):1376–1386.

    Article  PubMed  Google Scholar 

  36. Hoogendijk EO, Afilalo J, Ensrud KE, Kowal P, Onder G, Fried LP. Frailty: implications for clinical practice and public health. Lancet. 2019;394(10206):1365–1375.

    Article  PubMed  Google Scholar 

  37. Kong LN, Lyu Q, Yao HY, Yang L, Chen SZ. The prevalence of frailty among community-dwelling older adults with diabetes: A meta-analysis. Int J Nurs Stud. 2021;119:103952.

    Article  PubMed  Google Scholar 

  38. Li G, Prior JC, Leslie WD, et al. Frailty and risk of fractures in patients with type 2 diabetes. Diabetes Care. 2019;42(4):507–513.

    Article  PubMed  Google Scholar 

  39. Benetos A, Petrovic M, Strandberg T. Hypertension management in older and frail older patients. Circ Res. 2019;124(7):1045–1060.

    Article  CAS  PubMed  Google Scholar 

  40. Guasti L, Ambrosetti M, Ferrari M, et al. Management of hypertension in the elderly and frail patient. Drugs Aging. 2022;39(10):763–772.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Denfeld QE, Winters-Stone K, Mudd JO, Gelow JM, Kurdi S, Lee CS. The prevalence of frailty in heart failure: A systematic review and meta-analysis. Int J Cardiol. 2017;236:283–289.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Pandey A, Kitzman D, Reeves G. Frailty is intertwined with heart failure: mechanisms, prevalence, prognosis, assessment, and management. JACC Heart Fail. 2019;7(12):1001–1011.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Balducci L, Extermann M. Management of cancer in the older person: a practical approach. Oncologist. 2000;5(3):224–237.

    Article  CAS  PubMed  Google Scholar 

  44. Handforth C, Clegg A, Young C, et al. The prevalence and outcomes of frailty in older cancer patients: a systematic review. Ann Oncol. 2015;26(6):1091–1101.

    Article  CAS  PubMed  Google Scholar 

  45. Wang S, Yang T, Qiang W, et al. The prevalence of frailty among breast cancer patients: a systematic review and meta-analysis. Support Care Cancer. 2022;30(4):2993–3006.

    Article  PubMed  Google Scholar 

  46. Komici K, Bencivenga L, Navani N, et al. Frailty in patients with lung cancer: a systematic review and meta-analysis. Chest. 2022;162(2):485–497.

    Article  PubMed  Google Scholar 

  47. Ferrucci L, Fabbri E. Inflammageing: Chronic inflammation in ageing, cardiovascular disease, and frailty. Nat Rev Cardiol. 2018;15(9):505–522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Wilson D, Jackson T, Sapey E, Lord JM. Frailty and sarcopenia: the potential role of an aged immune system. Ageing Res Rev. 2017;36:1–10.

    Article  PubMed  Google Scholar 

  49. Padoan A, Plebani M, Basso D. Inflammation and pancreatic cancer: focus on metabolism, cytokines, and immunity. Int J Mol Sci. 2019;20(3).

  50. Subramaniam S, Aalberg JJ, Soriano RP, Divino CM. New 5-factor modified frailty index using american college of surgeons NSQIP data. J Am Coll Surg. 2018;226(2):173–181.e178.

    Article  PubMed  Google Scholar 

  51. Hamaker ME, Jonker JM, de Rooij SE, Vos AG, Smorenburg CH, van Munster BC. Frailty screening methods for predicting outcome of a comprehensive geriatric assessment in elderly patients with cancer: a systematic review. Lancet Oncol. 2012;13(10):e437–444.

    Article  PubMed  Google Scholar 

  52. Meldon SW, Mion LC, Palmer RM, et al. A brief risk-stratification tool to predict repeat emergency department visits and hospitalizations in older patients discharged from the emergency department. Acad Emerg Med. 2003;10(3):224–232.

    PubMed  Google Scholar 

  53. Shaw JF, Budiansky D, Sharif F, McIsaac DI. The association of frailty with outcomes after cancer surgery: a systematic review and metaanalysis. Ann Surg Oncol. 2022;29(8):4690–4704.

    Article  PubMed  Google Scholar 

  54. Shinall MC Jr, Arya S, Youk A, et al. Association of preoperative patient frailty and operative stress with postoperative mortality. JAMA Surg. 2020;155(1):e194620.

    Article  PubMed  Google Scholar 

  55. Kennedy CA, Shipway D, Barry K. Frailty and emergency abdominal surgery: a systematic review and meta-analysis. Surgeon. 2022;20(6):e307–e314.

    Article  PubMed  Google Scholar 

  56. Hanlon P, Nicholl BI, Jani BD, Lee D, McQueenie R, Mair FS. Frailty and pre-frailty in middle-aged and older adults and its association with multimorbidity and mortality: a prospective analysis of 493 737 UK Biobank participants. Lancet Public Health. 2018;3(7):e323–e332.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Mintziras I, Miligkos M, Wächter S, Manoharan J, Maurer E, Bartsch DK. Sarcopenia and sarcopenic obesity are significantly associated with poorer overall survival in patients with pancreatic cancer: systematic review and meta-analysis. Int J Surg. 2018;59:19–26.

    Article  PubMed  Google Scholar 

  58. Rom H, Tamir S, Van Vugt JLA, et al. Sarcopenia as a predictor of survival in patients with pancreatic adenocarcinoma after pancreatectomy. Ann Surg Oncol. 2022;29(3):1553–1563.

    Article  PubMed  Google Scholar 

  59. Hurst C, Robinson SM, Witham MD, et al. Resistance exercise as a treatment for sarcopenia: Prescription and delivery. Age Ageing 2022;51(2).

  60. Sayer AA, Cruz-Jentoft A. Sarcopenia definition, diagnosis and treatment: Consensus is growing. Age Ageing. 2022;51(10).

Download references

Acknowledgements

F.Z. takes responsibility for the manuscript data and analysis content. F.Z. and C.G. were responsible for conceptualization and study design. F.Z. and Y.Y. were responsible for data acquisition, curation, and analysis. F.Z. participated in the manuscript writing. All authors had full access to all the data in the study, participated in data interpretation, revised the manuscript, and approved the final version for publication.

Author information

Authors and Affiliations

  1. Department of Hepatobiliary and Pancreatic Surgery, Hunnan Division of the First Hospital of China Medical University, Shenyang, China

    Fei Zhang MD, MPH & Chunlin Ge MD

  2. Department of Urinary Surgery, Northeast International Hospital, Shenyang, China

    Ying Yan BN

Authors
  1. Fei Zhang MD, MPH
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ying Yan BN
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chunlin Ge MD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fei Zhang MD, MPH.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, F., Yan, Y. & Ge, C. Prevalence and Impact of Frailty in Pancreatic Cancer: A Systematic Review and Meta-Analysis Based on 35,191 Patients. Ann Surg Oncol 31, 535–544 (2024). https://doi.org/10.1245/s10434-023-14426-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-023-14426-y

Keywords

Search

Navigation