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Cognitive impairment in candidates for allogeneic hematopoietic stem cell transplantation

Abstract

Hematopoietic cell transplant (HCT) is an increasingly common and curative treatment strategy to improve survival among individuals with malignant and nonmalignant diseases, with over one million HCTs having been performed worldwide. Neurocognitive dysfunction is a common and untoward consequence of HCT for many recipients, although few studies have examined the profile of neurocognitive impairments in HCT or their association with clinical features, such as frailty, or the incidence of pre-HCT neurocognitive impairments across all ages, which may influence post-HCT neurocognitive impairments. We examined the pattern and correlates of pre-transplant neurocognitive dysfunction in a prospective sample of adults undergoing HCT. Neurocognition was assessed using the Montreal Cognitive Assessment Battery. Frailty was assessed using the Short Physical Performance Battery. Linear regression analysis was used to examine the associations between neurocognitive performance and frailty. Neurocognitive screening profiles were also examined by partitioning MoCA into domain scores, including Executive Function and Memory. We also examined the associations between neurocognition, frailty, and clinical outcomes, including length of transplant hospitalization and survival. One hundred and ten adults were evaluated across a wide age range (range: 19–75; mean age = 54.7 [SD = 14.1]). Neurocognitive performance tended to fall below published normative levels (mean MoCA = 25.5 [SD = 4.1]), with 17% of participants demonstrating impaired performance compared with medical normative data (MoCA ≤ 22) and 34% exhibiting impaired performance relative to healthy samples (MoCA ≤ 25). Mild impairments (MoCA ≤ 25) were common across age ranges, including middle-aged patients (23% for age < 50; 35% for age 50–60, 41% for age ≥ 60), particularly for items assessing Executive Function. Greater levels of frailty associated with lower neurocognitive screening scores (r = −0.29, P < 0.01) and Executive Functioning (r = −0.24, P < 0.01), whereas greater age was associated with poorer Memory performance only (r = −0.33, P < 0.01). Greater levels of frailty prior to transplant associated with longer length of stay (β = 0.10, P = 0.046), but were not associated with survival. Neurocognitive impairments are common among adults undergoing HCT and the pattern of performance varies by age. Pre-transplant frailty is associated with neurocognitive functioning and may portend worse post-transplant early clinical outcomes.

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Fig. 1: Frailty and cognitive functioning.

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References

  1. Abel GA, Buckstein R. Integrating Frailty, Comorbidity, and Quality of Life in the Management of Myelodysplastic Syndromes. Am Soc Clin Oncol Educ Book. 2016;35:e337–344. https://doi.org/10.14694/EDBK_158639. 10.1200/EDBK_158639.

    Article  PubMed  Google Scholar 

  2. Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C, et al. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the american heart association/american stroke association. Stroke. 2011;42:2672–713. https://doi.org/10.1161/STR.0b013e3182299496. e-pub ahead of print 2011/07/23.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Barnes DE, Yaffe K. The projected effect of risk factor reduction on Alzheimer’s disease prevalence. Lancet Neurol. 2011;10:819–28.

    Article  Google Scholar 

  4. Plassman BL, Williams JW, Burke JR, Holsinger T, Benjamin S. Systematic review: factors associated with risk for and possible prevention of cognitive decline in later life. Ann Intern Med. 2010;153:182–93.

    Article  Google Scholar 

  5. Kelly DL, Buchbinder D, Duarte RF, Auletta JJ, Bhatt N, Byrne M, et al. Neurocognitive Dysfunction in Hematopoietic Cell Transplant Recipients: Expert Review from the Late Effects and Quality of Life Working Committee of the Center for International Blood and Marrow Transplant Research and Complications and Quality of Life Working Party of the European Society for Blood and Marrow Transplantation. Biol Blood Marrow Transpl. 2018;24:228–41. https://doi.org/10.1016/j.bbmt.2017.09.004.

    Article  Google Scholar 

  6. Buchbinder D, Kelly DL, Duarte RF, Auletta JJ, Bhatt N, Byrne M, et al. Neurocognitive dysfunction in hematopoietic cell transplant recipients: expert review from the late effects and Quality of Life Working Committee of the CIBMTR and complications and Quality of Life Working Party of the EBMT. Bone Marrow Transpl. 2018;53:535–55. https://doi.org/10.1038/s41409-017-0055-7.

    Article  CAS  Google Scholar 

  7. Holmes HM, Des Bordes JK, Kebriaei P, Yennu S, Champlin RE, Giralt S, et al. Optimal screening for geriatric assessment in older allogeneic hematopoietic cell transplantation candidates. J Geriatr Oncol. 2014;5:422–30. https://doi.org/10.1016/j.jgo.2014.04.004.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Muffly LS, Kocherginsky M, Stock W, Chu Q, Bishop MR, Godley LA, et al. Geriatric assessment to predict survival in older allogeneic hematopoietic cell transplantation recipients. Haematologica. 2014;99:1373–9. https://doi.org/10.3324/haematol.2014.103655.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Fraz MA, Warraich FH, Warraich SU, Tariq MJ, Warraich Z, Khan AY, et al. Special considerations for the treatment of multiple myeloma according to advanced age, comorbidities, frailty and organ dysfunction. Crit Rev Oncol Hematol. 2019;137:18–26. https://doi.org/10.1016/j.critrevonc.2019.02.011.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Atakul E, Akyar I. Frailty Prevalence and Characteristics in Older Adults with Hematologic Cancer: a Descriptive Study. Asia Pac J Oncol Nurs. 2019;6:43–9. https://doi.org/10.4103/apjon.apjon_35_18.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hegde A, Murthy HS. Frailty: the missing piece of the pre- hematopoietic cell transplantation assessment? Bone Marrow Transpl. 2018;53:3–10. https://doi.org/10.1038/bmt.2017.192.

    Article  CAS  Google Scholar 

  12. Arora M, Sun CL, Ness KK, Teh JB, Wu J, Francisco L, et al. Physiologic Frailty in Nonelderly Hematopoietic Cell Transplantation Patients: results From the Bone Marrow Transplant Survivor Study. JAMA Oncol. 2016;2:1277–86. https://doi.org/10.1001/jamaoncol.2016.0855.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Quinlan N, Marcantonio ER, Inouye SK, Gill TM, Kamholz B, Rudolph JL. Vulnerability: the crossroads of frailty and delirium. J Am Geriatr Soc. 2011;59:S262–268. https://doi.org/10.1111/j.1532-5415.2011.03674.x. Suppl 2.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Bellelli G, Moresco R, Panina-Bordignon P, Arosio B, Gelfi C, Morandi A, et al. Is Delirium the Cognitive Harbinger of Frailty in Older Adults? A Review about the Existing Evidence. Front Med (Lausanne). 2017;4:188. https://doi.org/10.3389/fmed.2017.00188.

    Article  Google Scholar 

  15. Sargent L, Nalls M, Amella EJ, Slattum PW, Mueller M, Bandinelli S, et al. Shared mechanisms for cognitive impairment and physical frailty: A model for complex systems. Alzheimers Dement (N.Y). 2020;6:e12027. https://doi.org/10.1002/trc2.12027. e-pub ahead of print 2020/07/21.

    Article  Google Scholar 

  16. Mayo S, Messner HA, Rourke SB, Howell D, Victor JC, Kuruvilla J, et al. Relationship between neurocognitive functioning and medication management ability over the first 6 months following allogeneic stem cell transplantation. Bone Marrow Transpl. 2016;51:841–7. https://doi.org/10.1038/bmt.2016.2.

    Article  CAS  Google Scholar 

  17. Rodrigues M, de Souza PMR, de Oliveira Muniz Koch L, Hamerschlak N. The use of comprehensive geriatric assessment in older patients before allologeneic hematopoietic stem cell transplantation: a cross-sectional study. J Geriatr Oncol. 2020;11:100–6. https://doi.org/10.1016/j.jgo.2019.05.022. e-pub ahead of print 2019/06/25.

    Article  PubMed  Google Scholar 

  18. Pavasini R, Guralnik J, Brown JC, di Bari M, Cesari M, Landi F, et al. Short Physical Performance Battery and all-cause mortality: systematic review and meta-analysis. BMC Med. 2016;14:215. https://doi.org/10.1186/s12916-016-0763-7.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Guralnik JM, Ferrucci L, Pieper CF, Leveille SG, Markides KS, Ostir GV, et al. Lower extremity function and subsequent disability: consistency across studies, predictive models, and value of gait speed alone compared with the short physical performance battery. J Gerontol A Biol Sci Med Sci. 2000;55:M221–231. https://doi.org/10.1093/gerona/55.4.m221.

    Article  CAS  PubMed  Google Scholar 

  20. Courtwright AM, Zaleski D, Tevald M, Adler J, Singer JP, Cantu EE, et al. Discharge frailty following lung transplantation. Clin Transpl. 2019:e13694. https://doi.org/10.1111/ctr.13694.

  21. Venado A, McCulloch C, Greenland JR, Katz P, Soong A, Shrestha P, et al. Frailty trajectories in adult lung transplantation: a cohort study. J Heart Lung Transpl. 2019;38:699–707. https://doi.org/10.1016/j.healun.2019.03.006.

    Article  Google Scholar 

  22. Williams FR, Vallance A, Faulkner T, Towey J, Durman S, Kyte D, et al. Home-Based Exercise in Patients Awaiting Liver Transplantation: a feasibility study. Liver Transpl. 2019;25:995–1006. https://doi.org/10.1002/lt.25442.

    Article  PubMed  Google Scholar 

  23. Rozenberg D, Mathur S, Wickerson L, Chowdhury NA, Singer LG. Frailty and clinical benefits with lung transplantation. J Heart Lung Transpl. 2018;37:1245–53. https://doi.org/10.1016/j.healun.2018.06.005.

    Article  Google Scholar 

  24. Singer JP, Soong A, Bruun A, Bracha A, Chin G, Hays SR, et al. A mobile health technology enabled home-based intervention to treat frailty in adult lung transplant candidates: a pilot study. Clin Transpl. 2018;32:e13274. https://doi.org/10.1111/ctr.13274.

    Article  Google Scholar 

  25. Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF, Blazer DG, et al. A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol. 1994;49:M85–94.

    Article  CAS  Google Scholar 

  26. Perracini MR, Mello M, de Oliveira Maximo R, Bilton TL, Ferriolli E, Lustosa LP, et al. Diagnostic Accuracy of the Short Physical Performance Battery for Detecting Frailty in Older People. Phys Ther. 2020;100:90–8. https://doi.org/10.1093/ptj/pzz154. e-pub ahead of print 2019/10/16.

    Article  PubMed  Google Scholar 

  27. Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53:695–9.

    Article  Google Scholar 

  28. Smith T, Gildeh N, Holmes C. The Montreal Cognitive Assessment: validity and utility in a memory clinic setting. Can J Psychiatry Rev Canadienne de Psychiatr. 2007;52:329–32.

    Google Scholar 

  29. Wefel JS, Vardy J, Ahles T, Schagen SB. International Cognition and Cancer Task Force recommendations to harmonise studies of cognitive function in patients with cancer. Lancet Oncol. 2011;12:703–8. https://doi.org/10.1016/S1470-2045(10)70294-1. e-pub ahead of print 2011/03/01.

    Article  PubMed  Google Scholar 

  30. Koll TT, Sheese AN, Semin J, Ernst W, High R, Wildes TM, et al. Screening for cognitive impairment in older adults with hematological malignancies using the Montreal Cognitive Assessment and neuropsychological testing. J Geriatr Oncol. 2020;11:297–303. https://doi.org/10.1016/j.jgo.2019.11.007. e-pub ahead of print 2019/12/14.

    Article  PubMed  Google Scholar 

  31. Smith PJ, Blumenthal JA, Hoffman BM, Davis RD, Palmer SM. Postoperative cognitive dysfunction and mortality following lung transplantation. Am J Transpl. 2018;18:696–703. https://doi.org/10.1111/ajt.14570.

    Article  CAS  Google Scholar 

  32. Roman DD, Holker EG, Missov E, Colvin MM, Menk J. Neuropsychological functioning in heart transplant candidates. Clin Neuropsychol. 2016:1–20. https://doi.org/10.1080/13854046.2016.1212096.

  33. Bhat G, Yost G, Mahoney E. Cognitive function and left ventricular assist device implantation. J Heart Lung Transpl. 2015;34:1398–405. https://doi.org/10.1016/j.healun.2015.05.015.

    Article  Google Scholar 

  34. Montero-Odasso M, Almeida QJ, Bherer L, Burhan AM, Camicioli R, Doyon J, et al. Consensus on Shared Measures of Mobility and Cognition: from the Canadian Consortium on Neurodegeneration in Aging (CCNA). J Gerontol A Biol Sci Med Sci. 2019;74:897–909. https://doi.org/10.1093/gerona/gly148. e-pub ahead of print 2018/08/14.

    Article  PubMed  Google Scholar 

  35. Montero-Odasso M, Almeida QJ, Burhan AM, Camicioli R, Doyon J, Fraser S, et al. SYNERGIC TRIAL (SYNchronizing Exercises, Remedies in Gait and Cognition) a multi-Centre randomized controlled double blind trial to improve gait and cognition in mild cognitive impairment. BMC Geriatr. 2018;18:93. https://doi.org/10.1186/s12877-018-0782-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Bartoli M, Palermo S, Cipriani GE, Amanzio M. A Possible Association Between Executive Dysfunction and Frailty in Patients With Neurocognitive Disorders. Front Psychol. 2020;11:554307. https://doi.org/10.3389/fpsyg.2020.554307. e-pub ahead of print 2020/12/03.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Lorenzo-Lopez L, Blanco-Fandino J, Cibeira N, Bujan A, Lopez-Lopez R, Maseda A, et al. Clinical and Neuropsychological Correlates of Prefrailty Syndrome. Front Med (Lausanne). 2020;7:609359. https://doi.org/10.3389/fmed.2020.609359. e-pub ahead of print 2020/11/27.

    Article  Google Scholar 

  38. Yoon DH, Lee JY, Song W. Effects of Resistance Exercise Training on Cognitive Function and Physical Performance in Cognitive Frailty: a Randomized Controlled Trial. J Nutr Health Aging. 2018;22:944–51. https://doi.org/10.1007/s12603-018-1090-9.

    Article  CAS  PubMed  Google Scholar 

  39. Coen RF, Robertson DA, Kenny RA, King-Kallimanis BL. Strengths and Limitations of the MoCA for Assessing Cognitive Functioning: findings From a Large Representative Sample of Irish Older Adults. J Geriatr Psychiatry Neurol. 2016;29:18–24. https://doi.org/10.1177/0891988715598236. e-pub ahead of print 2015/08/08.

    Article  PubMed  Google Scholar 

  40. Freitas S, Simoes MR, Maroco J, Alves L, Santana I. Construct Validity of the Montreal Cognitive Assessment (MoCA). J Int Neuropsychol Soc. 2012;18:242–50. https://doi.org/10.1017/S1355617711001573. e-pub ahead of print 2011/11/26.

    Article  PubMed  Google Scholar 

  41. Duro D, Simoes MR, Ponciano E, Santana I. Validation studies of the Portuguese experimental version of the Montreal Cognitive Assessment (MoCA): confirmatory factor analysis. J Neurol. 2010;257:728–34. https://doi.org/10.1007/s00415-009-5399-5. e-pub ahead of print 2009/11/26.

    Article  PubMed  Google Scholar 

  42. Smith CR, Cavanagh J, Sheridan M, Grosset KA, Cullen B, Grosset DG. Factor structure of the Montreal Cognitive Assessment in Parkinson disease. Int J Geriatr Psychiatry. 2020;35:188–94. https://doi.org/10.1002/gps.5234. e-pub ahead of print 2019/11/19.

    Article  PubMed  Google Scholar 

  43. Spano G, Caffo AO, Lanciano T, Curci A, Bosco A. Visuospatial/executive abilities and mood affect the reliability of a subjective memory complaints measure. Aging Clin Exp Res. 2020;32:1317–26. https://doi.org/10.1007/s40520-019-01307-2. e-pub ahead of print 2019/08/21.

    Article  PubMed  Google Scholar 

  44. Benge JF, Balsis S, Madeka T, Uhlman C, Lantrip C, Soileau MJ. Factor structure of the Montreal Cognitive Assessment items in a sample with early Parkinson’s disease. Parkinsonism Relat Disord. 2017;41:104–8. https://doi.org/10.1016/j.parkreldis.2017.05.023. e-pub ahead of print 2017/06/03.

    Article  PubMed  Google Scholar 

  45. Foster R, Walker S, Brar R, Hiebert B, Komenda P, Rigatto C, et al. Cognitive Impairment in Advanced Chronic Kidney Disease: The Canadian Frailty Observation and Interventions Trial. Am J Nephrol. 2016;44:473–80. https://doi.org/10.1159/000450837. e-pub ahead of print 2016/11/01.

    Article  PubMed  Google Scholar 

  46. Pendlebury ST, Cuthbertson FC, Welch SJ, Mehta Z, Rothwell PM. Underestimation of cognitive impairment by mini-mental state examination versus the montreal cognitive assessment in patients with transient ischemic attack and stroke: a population-based study. Stroke. 2010;41:1290–3.

    Article  Google Scholar 

  47. Phillips KM, McGinty HL, Cessna J, Asvat Y, Gonzalez B, Cases MG, et al. A systematic review and meta-analysis of changes in cognitive functioning in adults undergoing hematopoietic cell transplantation. Bone Marrow Transpl. 2013;48:1350–7. https://doi.org/10.1038/bmt.2013.61.

    Article  CAS  Google Scholar 

  48. Smith PJ, Rivelli S, Waters A, Reynolds J, Hoyle A, Flowers M, et al. Neurocognitive changes after lung transplantation. Ann Am Thorac Soc. 2014;11:1520–7. https://doi.org/10.1513/AnnalsATS.201406-232OC.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Smith PJ, Blumenthal JA, Carney RM, Freedland KE, O’Hayer CVF, Trulock EP, et al. Neurobehavioral functioning and survival following lung transplantation. Chest. 2014;145:604–11. https://doi.org/10.1378/chest.12-2127.

    Article  PubMed  Google Scholar 

  50. Dew MA, DiMartini AF, Dobbels F, Grady KL, Jowsey-Gregoire SG, Kaan A, et al. The 2018 ISHLT/APM/AST/ICCAC/STSW recommendations for the psychosocial evaluation of adult cardiothoracic transplant candidates and candidates for long-term mechanical circulatory support. J Heart Lung Transpl. 2018;37:803–23. https://doi.org/10.1016/j.healun.2018.03.005.

    Article  Google Scholar 

  51. Panza F, D’Introno A, Colacicco AM, Capurso C, Parigi AD, Capurso SA, et al. Cognitive frailty: Predementia syndrome and vascular risk factors. Neurobiol Aging. 2006;27:933–40.

    Article  CAS  Google Scholar 

  52. Aliberti MJR, Cenzer IS, Smith AK, Lee SJ, Yaffe K, Covinsky KE. Assessing Risk for Adverse Outcomes in Older Adults: the Need to Include Both Physical Frailty and Cognition. J Am Geriatr Soc. 2019;67:477–83. https://doi.org/10.1111/jgs.15683.

    Article  PubMed  Google Scholar 

  53. Peng LN, Chou MY, Liang CK, Lee WJ, Kojima T, Lin MH, et al. Association between serum activin A and metabolic syndrome in older adults: Potential of activin A as a biomarker of cardiometabolic disease. Exp Gerontol. 2018;111:197–202. https://doi.org/10.1016/j.exger.2018.07.020.

    Article  CAS  PubMed  Google Scholar 

  54. Liu Z, Hsu FC, Trombetti A, King AC, Liu CK, Manini TM, et al. Effect of 24-month physical activity on cognitive frailty and the role of inflammation: the LIFE randomized clinical trial. BMC Med. 2018;16:185. https://doi.org/10.1186/s12916-018-1174-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Summers MJ, Rainero I, Vercelli AE, Aumayr G, de Rosario H, Monter M, et al. The My Active and Healthy Aging (My-AHA) ICT platform to detect and prevent frailty in older adults: Randomized control trial design and protocol. Alzheimers Dement (N. Y). 2018;4:252–62. https://doi.org/10.1016/j.trci.2018.06.004.

    Article  Google Scholar 

  56. Wood WA, Weaver M, Smith-Ryan AE, Hanson ED, Shea TC, Battaglini CL. Lessons learned from a pilot randomized clinical trial of home-based exercise prescription before allogeneic hematopoietic cell transplantation. Support Care Cancer. 2020;28:5291–8. https://doi.org/10.1007/s00520-020-05369-1. e-pub ahead of print 2020/03/01.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Rupnik E, Skerget M, Sever M, Zupan IP, Ogrinec M, Ursic B, et al. Feasibility and safety of exercise training and nutritional support prior to haematopoietic stem cell transplantation in patients with haematologic malignancies. BMC Cancer. 2020;20:1142. https://doi.org/10.1186/s12885-020-07637-z. e-pub ahead of print 2020/11/26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Bongers BC, Klaase JM, van Meeteren NLU. Prehabilitation vs Postoperative Rehabilitation for Frail Patients. JAMA Surg. 2020;155:896–7. https://doi.org/10.1001/jamasurg.2020.1801. e-pub ahead of print 2020/06/26.

    Article  PubMed  Google Scholar 

  59. Gritsenko K, Helander E, Webb MPK, Okeagu CN, Hyatali F, Renschler JS, et al. Preoperative frailty assessment combined with prehabilitation and nutrition strategies: Emerging concepts and clinical outcomes. Best Pr Res Clin Anaesthesiol. 2020;34:199–212. https://doi.org/10.1016/j.bpa.2020.04.008. e-pub ahead of print 2020/07/28.

    Article  Google Scholar 

  60. Dezube AR, Cooper L, Jaklitsch MT. Prehabilitation of the Thoracic Surgery Patient. Thorac Surg Clin. 2020;30:249–58. https://doi.org/10.1016/j.thorsurg.2020.04.004. e-pub ahead of print 2020/07/01.

    Article  PubMed  Google Scholar 

  61. Norris CM, Close JCT. Prehabilitation for the frailty syndrome: improving outcomes for our most vulnerable patients. Anesth Analg. 2020;130:1524–33. https://doi.org/10.1213/ANE.0000000000004785. e-pub ahead of print 2020/05/10.

    Article  PubMed  Google Scholar 

  62. Subramaniam A, Tiruvoipati R, Lodge M, Moran C, Srikanth V. Frailty in the older person undergoing elective surgery: a trigger for enhanced multidisciplinary management - a narrative review. ANZ J Surg. 2020;90:222–9. https://doi.org/10.1111/ans.15633. e-pub ahead of print 2020/01/10.

    Article  PubMed  Google Scholar 

  63. Urits I, Orhurhu V, Jones M, Hoyt D, Seats A, Viswanath O. Current Perspectives on Postoperative Cognitive Dysfunction in the Ageing Population. Turk J Anaesthesiol Reanim. 2019;47:439–47. https://doi.org/10.5152/TJAR.2019.75299. e-pub ahead of print 2019/12/13.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Kow AW. Prehabilitation and Its Role in Geriatric Surgery. Ann Acad Med Singap. 2019;48:386–92. e-pub ahead of print 2020/01/22.

  65. Czobor NR, Lehot JJ, Holndonner-Kirst E, Tully PJ, Gal J, Szekely A. Frailty In Patients Undergoing Vascular Surgery: a Narrative Review Of Current Evidence. Ther Clin Risk Manag. 2019;15:1217–32. https://doi.org/10.2147/TCRM.S217717. e-pub ahead of print 2019/12/06.

    Article  PubMed  PubMed Central  Google Scholar 

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PJS collected the data, analyzed the data, wrote the paper, revised the paper, and secured funding for the project; ML collected the data, analyzed the data, revised the paper; YL collected the data, analyzed the data, and revised the paper; KR collected the data, analyzed the data, and revised the paper; JCT collected the data, analyzed the data, and revised the paper; LB collected the data, analyzed the data, and revised the paper; AP collected the data and revised the paper; AA collected the data, analyzed the data, and revised the paper; SR collected the data, analyzed the data, and revised the paper; TC revised the paper; CG revised the paper; MH revised the paper; GL revised the paper; RL revised the paper; DR revised the paper; SS revised the paper; KS revised the paper; NC revised the paper; ADS analyzed the data, revised the paper, and secured funding for the project.

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Smith, P.J., Lew, M., Lowder, Y. et al. Cognitive impairment in candidates for allogeneic hematopoietic stem cell transplantation. Bone Marrow Transplant 57, 89–94 (2022). https://doi.org/10.1038/s41409-021-01470-z

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