Skip to main content

Advertisement

SpringerLink
Log in

How, when, and why individuals with stage IV cancer seen in an outpatient setting are referred to palliative care: a mixed methods study

  • Original Article
  • Published:
Supportive Care in Cancer Aims and scope Submit manuscript

Abstract

Purpose

Early palliative care (PC) for individuals with advanced cancer improves patient and family outcomes and experience. However, it is unknown when, why, and how in an outpatient setting individuals with stage IV cancer are referred to PC.

Methods

At a large multi-specialty group in the USA with outpatient PC implemented beginning in 2011, clinical records were used to identify adults diagnosed with stage IV cancer after January 1, 2012 and deceased by December 31, 2017 and their PC referrals and hospice use. In-depth interviews were also conducted with 25 members of medical oncology, gynecological oncology, and PC teams and thematically analyzed.

Results

A total of 705 individuals were diagnosed and died between 2012 and 2017: of these, 332 (47%) were referred to PC, with 48.5% referred early (within 60 days of diagnosis). Among referred patients, 79% received hospice care, versus 55% among patients not referred. Oncologists varied dramatically in their rates of referral to PC. Interviews revealed four referral pathways: early referrals, referrals without active anti-cancer treatment, problem-based referrals, and late referrals (when stopping treatment). Participants described PC’s benefits as enhancing pain/symptom management, advance care planning, transitions to hospice, end-of-life experiences, a larger team, and more flexible patient care. Challenges reported included variation in oncologist practices, patient fears and misconceptions, and access to PC teams.

Conclusion

We found high rates of use and appreciation of PC. However, interviews revealed that exclusively focusing on rates of referrals may obscure how referrals vary in timing, reason for referral, and usefulness to patients, families, and clinical teams.

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

Similar content being viewed by others

References

  1. Ahluwalia SC, Fried TR (2009) Physician factors associated with outpatient palliative care referral. Palliat Med 23(7):608-615

  2. Bakitas MA, Tosteson TD, Li Z, Lyons KD, Hull JG, Li Z, Dionne-Odom JN, Frost J, Dragnev KH, Hegel MT (2015) Early versus delayed initiation of concurrent palliative oncology care: patient outcomes in the ENABLE III randomized controlled trial. J Clin Oncol 33:1438–1445

    Article  Google Scholar 

  3. Brand DA (2019) The stage IV shuffle: elusiveness of straight talk about advanced cancer. J Gen Intern Med. 34.11(2019):2637-2642

  4. Broom A, Kirby E, Good P, Wootton J, Adams J (2013) The art of letting go: referral to palliative care and its discontents. Soc Sci Med 78:9–16

    Article  Google Scholar 

  5. Center to Advance Palliative Care and the National Palliative Care Research Center. America’s Care of Serious Illness: a state-by-state report card on access to palliative care in our nation's hospitals. 2019

  6. Charmaz K (2017) The power of constructivist grounded theory for critical inquiry. Qual Inq 23:34–45

    Article  Google Scholar 

  7. Compton-Phillips A, Mohta NS (2019) Care redesign survey: the power of palliative care. NEJM Catalyst

  8. Courtright KR, Chivers C, Becker M, Regli SH, Pepper LC, Draugelis ME, O’Connor NR (2019) Electronic health record mortality prediction model for targeted palliative care among hospitalized medical patients: a pilot quasi-experimental study. J Gen Intern Med 34:1841–1847

    Article  Google Scholar 

  9. Dans M, Smith T, Back A, Baker JN, Bauman JR, Beck AC, Block S, Campbell T, Case AA, Dalal S, Edwards H, Fitch TR, Kapo J, Kutner JS, Kvale E, Miller C, Misra S, Mitchell W, Portman DG, Spiegel D, Sutton L, Szmuilowicz E, Temel J, Tickoo R, Urba SG, Weinstein E, Zachariah F, Bergman MA, Scavone JL (2017) NCCN guidelines insights: palliative care, version 2.2017. J Natl Compr Cancer Netw 15:989–997

    Article  Google Scholar 

  10. de Oliveira Valentino TC, Paiva BSR, de Oliveira MA, Hui D, Paiva CE (2018) Factors associated with palliative care referral among patients with advanced cancers: a retrospective analysis of a large Brazilian cohort. Support Care Cancer 26:1933–1941

    Article  Google Scholar 

  11. Fadul N, Elsayem A, Palmer JL, Del Fabbro E, Swint K, Li Z, Poulter V, Bruera E (2009) Supportive versus palliative care: what’s in a name? A survey of medical oncologists and midlevel providers at a comprehensive cancer center. Cancer 115:2013–2021

    Article  Google Scholar 

  12. Feeg VD, Elebiary H (2005) Exploratory study on end-of-life issues: barriers to palliative care and advance directives. Am J Hosp Palliat Care 22:119–124

    Article  Google Scholar 

  13. Ferrell BR, Temel JS, Temin S, Alesi ER, Balboni TA, Basch EM, Firn JI, Paice JA, Peppercorn JM, Phillips T (2017) Integration of palliative care into standard oncology care: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol 35:96–112

    Article  Google Scholar 

  14. Gemmell R, Yousaf N, Droney J (2019) “Triggers” for early palliative care referral in patients with cancer: a review of urgent unplanned admissions and outcomes. Support Care Cancer

  15. Glaser BG, Strauss AL (1968) The discovery of grounded theory: strategies for qualitative research. Weidenfeld and Nicolson, London

    Google Scholar 

  16. Greer JA, Jackson VA, Meier DE, Temel JS (2013) Early integration of palliative care services with standard oncology care for patients with advanced cancer. CA Cancer J Clin 63:349–363

    Article  Google Scholar 

  17. Greer JA, Pirl WF, Jackson VA, Muzikansky A, Lennes IT, Heist RS, Gallagher ER, Temel JS (2012) Effect of early palliative care on chemotherapy use and end-of-life care in patients with metastatic non-small-cell lung cancer. J Clin Oncol 30:394–400

    Article  Google Scholar 

  18. Guest G, Bunce A, Johnson L (2006) How many interviews are enough? An experiment with data saturation and variability. Field Methods 18:59–82

    Article  Google Scholar 

  19. Hui D, Anderson L, Tang M, Park M, Liu D, Bruera E (2020) Examination of referral criteria for outpatient palliative care among patients with advanced cancer. Support Care Cancer 28:295–301

    Article  Google Scholar 

  20. Hui D, Kim SH, Roquemore J, Dev R, Chisholm G, Bruera E (2014) Impact of timing and setting of palliative care referral on quality of end-of-life care in cancer patients. Cancer 120:1743–1749

    Article  Google Scholar 

  21. Jackson VA, Jacobsen J, Greer JA, Pirl WF, Temel JS, Back AL (2013) The cultivation of prognostic awareness through the provision of early palliative care in the ambulatory setting: a communication guide. J Palliat Med 16:894–900

    Article  Google Scholar 

  22. Jacobson JO (2019) Managing cancer patients' expectations amid hope and hype. Health Aff (Millwood) 38:320–323

    Article  Google Scholar 

  23. Jung K, Sudat SE, Kwon N, Stewart WF, Shah NH (2019) Predicting need for advanced illness or palliative care in a primary care population using electronic health record data. J Biomed Inform:103115

  24. Kamal AH, Wolf SP, Troy J, Leff V, Dahlin C, Rotella JD, Handzo G, Rodgers PE, Myers ER (2019) Policy changes key to promoting sustainability and growth of the specialty palliative care workforce. Health Aff (Millwood) 38:910–918

    Article  Google Scholar 

  25. Kavalieratos D, Mitchell EM, Carey TS, Dev S, Biddle AK, Reeve BB, Abernethy AP, Weinberger M (2014) “Not the ‘grim reaper service’”: an assessment of provider knowledge, attitudes, and perceptions regarding palliative care referral barriers in heart failure. Am Heart J 3:e000544

    Google Scholar 

  26. Kirby ER, Kenny KE, Broom AF, Oliffe JL, Lewis S, Wyld DK, Yates PM, Parker RB, Lwin Z (2020) Responses to a cancer diagnosis: a qualitative patient-centred interview study. Support Care Cancer 28:229–238

    Article  Google Scholar 

  27. Kleinman A (1988) The illness narratives: suffering, healing, and the human condition. Basic Books, New York

    Google Scholar 

  28. Le BH, Mileshkin L, Doan K, Saward D, Spruyt O, Yoong J, Gunawardana D, Conron M, Philip J (2014) Acceptability of early integration of palliative care in patients with incurable lung cancer. J Palliat Med 17:553–558

    Article  Google Scholar 

  29. LeBlanc T, Nickolich M, El-Jawahri A, Temel J (2015) Discussing the evidence for upstream palliative care in improving outcomes in advanced cancer. In: Editor (ed)^(eds) Book discussing the evidence for upstream palliative care in improving outcomes in advanced cancer, City, pp. e534-538

  30. Lupu D, American Academy of H, Palliative Medicine Workforce Task F (2010) Estimate of current hospice and palliative medicine physician workforce shortage. J Pain Symptom Manag 40:899–911

    Article  Google Scholar 

  31. Maciasz R, Arnold R, Chu E, Park S, White D, Vater L, Schenker Y (2013) Does it matter what you call it? A randomized trial of language used to describe palliative care services. Support Care Cancer 21:3411–3419

    Article  CAS  Google Scholar 

  32. Meier D, Beresford L (2008) Outpatient clinics are a new frontier for palliative care. J Palliat Med 11:823–828

    Article  Google Scholar 

  33. Muir JC, Daly F, Davis MS, Weinberg R, Heintz JS, Paivanas TA, Beveridge R (2010) Integrating palliative care into the outpatient, private practice oncology setting. J Pain Symptom Manag 40:126–135

    Article  Google Scholar 

  34. O'Brien BC, Harris IB, Beckman TJ, Reed DA, Cook DA (2014) Standards for reporting qualitative research: a synthesis of recommendations. Acad Med 89:1245–1251

    Article  Google Scholar 

  35. Rabow M, Kvale E, Barbour L, Cassel JB, Cohen S, Jackson V, Luhrs C, Nguyen V, Rinaldi S, Stevens D (2013) Moving upstream: a review of the evidence of the impact of outpatient palliative care. J Palliat Med 16:1540–1549

    Article  Google Scholar 

  36. Smith TJ, Temin S, Alesi ER, Abernethy AP, Balboni TA, Basch EM, Ferrell BR, Loscalzo M, Meier DE, Paice JA, Peppercorn JM, Somerfield M, Stovall E, Roenn JHV (2012) American Society of Clinical Oncology provisional clinical opinion: the integration of palliative care into standard oncology care. J Clin Oncol 30:880–887

    Article  Google Scholar 

  37. Sullivan DR, Chan B, Lapidus JA, Ganzini L, Hansen L, Carney PA, Fromme EK, Marino M, Golden SE, Vranas KC (2019) Association of early palliative care use with survival and place of death among patients with advanced lung cancer receiving care in the Veterans Health Administration. JAMA Oncol

  38. Temel JS, Greer JA, El-Jawahri A, Pirl WF, Park ER, Jackson VA, Back AL, Kamdar M, Jacobsen J, Chittenden EH, Rinaldi SP, Gallagher ER, Eusebio JR, Li Z, Muzikansky A, Ryan DP (2017) Effects of early integrated palliative care in patients with lung and gi cancer: a randomized clinical trial. J Clin Oncol 35:834–841

    Article  Google Scholar 

  39. Temel JS, Greer JA, Muzikansky A, Gallagher ER, Admane S, Jackson VA, Dahlin CM, Blinderman CD, Jacobsen J, Pirl WF, Billings JA, Lynch TJ (2010) Early palliative care for patients with metastatic non-small-cell lung cancer. N Engl J Med 363:733–742

    Article  CAS  Google Scholar 

  40. Vanbutsele G, Pardon K, Van Belle S, Surmont V, De Laat M, Colman R, Eecloo K, Cocquyt V, Geboes K, Deliens L (2018) Effect of early and systematic integration of palliative care in patients with advanced cancer: a randomised controlled trial. Lancet Oncol 19:394–404

    Article  Google Scholar 

  41. Weeks JC, Catalano PJ, Cronin A, Finkelman MD, Mack JW, Keating NL, Schrag D (2012) Patients’ expectations about effects of chemotherapy for advanced cancer. N Engl J Med 367:1616–1625

    Article  CAS  Google Scholar 

  42. Yoong J, Park ER, Greer JA, Jackson VA, Gallagher ER, Pirl WF, Back AL, Temel JS (2013) Early palliative care in advanced lung cancer: a qualitative study. JAMA Intern Med 173:283–290

    Article  Google Scholar 

  43. Yu JA, Ray KN, Park SY, Barry A, Smith CB, Ellis PG, Schenker Y (2018) System-level factors associated with use of outpatient specialty palliative care among patients with advanced cancer. J Oncol Pract 15:e10–e19

    Article  Google Scholar 

  44. Zimmermann C, Swami N, Krzyzanowska M, Hannon B, Leighl N, Oza A, Moore M, Rydall A, Rodin G, Tannock I (2014) Early palliative care for patients with advanced cancer: a cluster-randomised controlled trial. Lancet 383:1721–1730

    Article  Google Scholar 

Download references

Acknowledgments

We acknowledge and thank Pragati Kenkare, Mai Vu, and Lydia Jacobs for their support accessing data required for this analysis. We thank Yan Yang and Qiwen Huang for data analysis support. We thank members of the Palo Alto Medical Foundation medical oncology and palliative care teams for their help and participation in these interviews.

Authors’ contribution statements

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Ellis Dillon, Jinnan Li, Amy Meehan, and Nina Szwerinski. The first draft of the manuscript was written by Ellis Dillon, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Data and/or code availability

The authors do not have permission to share the electronic health record dataset or interview transcript dataset. Requests to see further data can be directed to the corresponding author.

Funding

This research was supported by funding from the Palo Alto Medical Foundation Philanthropy Department.

Author information

Authors and Affiliations

  1. Center for Health Systems Research, Sutter Health, Palo Alto, CA, USA

    Ellis C. Dillon, Amy Meehan, Su-Ying Liang, Nina K. Szwerinski & Hal Luft

  2. Palo Alto Medical Foundation Research Institute, 795 El Camino Real, Palo Alto, CA, 94301, USA

    Ellis C. Dillon, Amy Meehan, Su-Ying Liang, Nina K. Szwerinski & Hal Luft

  3. Lilly Suzhou Pharmaceutical Co. Ltd, Shanghai, China

    Jinnan Li

  4. formerly at Palo Alto Medical Foundation Research Institute, Palo Alto, CA, USA

    Jinnan Li

  5. Palo Alto Medical Foundation, Palo Alto, CA, USA

    Steve Lai, Natalia Colocci & Julie Roth

Authors
  1. Ellis C. Dillon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amy Meehan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jinnan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Su-Ying Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Steve Lai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Natalia Colocci
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Julie Roth
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Nina K. Szwerinski
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hal Luft
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ellis C. Dillon.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

The Sutter Health Institutional Review Board approved this research study including the retrospective analysis of Electronic Health Record data and the in-depth interviews with clinical care team members.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 19 kb)

ESM 2

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dillon, E.C., Meehan, A., Li, J. et al. How, when, and why individuals with stage IV cancer seen in an outpatient setting are referred to palliative care: a mixed methods study. Support Care Cancer 29, 669–678 (2021). https://doi.org/10.1007/s00520-020-05492-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00520-020-05492-z

Keywords

Search

Navigation