Skip to main content

Risk stratification for clinical severity of pulmonary embolism in patients with cancer: a narrative review and MASCC clinical guidance for daily care

Abstract

Pulmonary embolism (PE) is a leading cause of morbidity and mortality in patients with cancer. The clinical presentation and outcomes of PE range from an acute life-threatening condition requiring intensive care to a mild symptomatic condition associated with favorable outcomes and potentially candidate for early hospital discharge. The wide clinical spectrum of PE has led to the development of risk stratification models aimed at the triage of patients in emergency care departments and optimizing the utilization of health care resources. Incidental or unsuspected PE (UPE), detected during routine staging computed tomography scans, make up a significant proportion of this cohort among the oncology population. The present narrative review is aimed at examining the currently available PE risk assessment models developed for the general population and for patients with cancer including UPE. We include general recommendations for the daily care of patients with cancer-related PE and hypothesize on the factors that would potentially favor hospitalization with early discharge or ambulatory management in this setting.

This is a preview of subscription content, access via your institution.

Fig. 1

Data availability

Not applicable.

Code availability

Not applicable.

References

  1. Khorana AA, Francis CW, Culakova E, Kuderer NM, Lyman GH (2007) Thromboembolism is a leading cause of death in cancer patients receiving outpatient chemotherapy. J Thromb Haemost 5:632–634

    CAS  PubMed  Article  Google Scholar 

  2. Sørensen HT, Mellemkjaer L, Olsen JH, Baron JA (2000) Prognosis of cancers associated with venous thromboembolism. N Engl J Med 343:1846–1850

    PubMed  Article  Google Scholar 

  3. Prandoni P, Lensing AW, Piccioli A et al (2002) Recurrent venous thromboembolism and bleeding complications during anticoagulant treatment in patients with cancer and venous thrombosis. Blood 100:3484–3488

    CAS  PubMed  Article  Google Scholar 

  4. Timp JF, Braekkan SK, Versteeg HH, Cannegieter SC (2013) Epidemiology of cancer-associated venous thrombosis. Blood 122:1712–1723

    CAS  PubMed  Article  Google Scholar 

  5. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A et al (2021) Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249

    PubMed  Article  Google Scholar 

  6. Browne AM, Cronin CG, English C, NiMhuircheartaigh J, Murphy JM, Bruzzi JF (2010) Unsuspected pulmonary emboli in oncology patients undergoing routine computed tomography imaging. J Thorac Oncol 5:798–803

    PubMed  Article  Google Scholar 

  7. Tapson VF (2008) Acute pulmonary embolism. N Engl J Med 6(358):1037–1052

    Article  Google Scholar 

  8. Agnelli G, Becattini C (2010) Acute pulmonary embolism. N Engl J Med 363:266–274

    CAS  PubMed  Article  Google Scholar 

  9. Cooksley T, Rice T (2017) Emergency oncology: development, current position and future direction in the USA and UK. Support Care Cancer 25:3–7

    PubMed  Article  Google Scholar 

  10. Todd KH, Thomas CR Jr (2016) An inflection point in the evolution of oncologic emergency medicine. Ann Emerg Med 68:712–716

    PubMed  Article  Google Scholar 

  11. Berman R, Davies A, Cooksley T, Gralla R, Carter L, Darlington E et al (2020) Supportive care: an indispensable component of modern oncology. Clin Oncol 32:781–788

    CAS  Article  Google Scholar 

  12. Hui D, Bruera E (2016) Integrating palliative care into the trajectory of cancer care. Nat Rev Clin Oncol 13:159–171

    PubMed  Article  Google Scholar 

  13. Martinez Licha CR, McCurdy CM, Maldonado SM, Lee LS (2020) Current management of acute pulmonary embolism. Ann Thorac Cardiovasc Surg 26:65–71

    PubMed  Article  Google Scholar 

  14. Konstantinides SV, Meyer G, Becattini C, Bueno H, Geersing GJ, Harjola VP et al (2020) 2019 ESC Guidelines for the diagnosis and management of acute pulmonary embolism developed in collaboration with the European Respiratory Society (ERS). Eur Heart J 41:543–603

    PubMed  Article  Google Scholar 

  15. Quezada CA, Bikdeli B, Barrios D, Barbero E, Chiluiza D, Muriel A et al (2019) Meta-analysis of prevalence and short-term prognosis of hemodynamically unstable patients with symptomatic acute pulmonary embolism. Am J Cardiol 123:684–689

    PubMed  Article  Google Scholar 

  16. Mikkola KM, Patel SR, Parker JA, Grodstein F, Goldhaber SZ (1997) Attenuation over 24 hours of the efficacy of thrombolysis of pulmonary embolism among patients with cancer. Am Heart J 134:603–607

    CAS  PubMed  Article  Google Scholar 

  17. Kurnicka K, Lichodziejewska B, Goliszek S, Dzikowska-Diduch O, Zdończyk O, Kozłowska M et al (2016) Echocardiographic pattern of acute pulmonary embolism: analysis of 511 consecutive patients. J Am Soc Echocardiogr 29:907–913

    PubMed  Article  Google Scholar 

  18. Meinel FG, Nance JW Jr, Schoepf UJ, Hoffmann VS, Thierfelder KM, Costello P et al (2015) Predictive value of computed tomography in acute pulmonary embolism: systematic review and meta-analysis. Am J Med 128:747-759.e2

    PubMed  Article  Google Scholar 

  19. Sanchez O, Trinquart L, Colombet I, Durieux P, Huisman MV, Chatellier G et al (2008) Prognostic value of right ventricular dysfunction in patients with haemodynamically stable pulmonary embolism: a systematic review. Eur Heart J 29:1569–1577

    PubMed  Article  Google Scholar 

  20. Coutance G, Cauderlier E, Ehtisham J, Hamon M, Hamon M (2011) The prognostic value of markers of right ventricular dysfunction in pulmonary embolism: a meta-analysis. Crit Care 15:R103

    PubMed  PubMed Central  Article  Google Scholar 

  21. Wicki J, Perrier A, Perneger TV, Bounameaux H, Junod AF (2000) Predicting adverse outcome in patients with acute pulmonary embolism: a risk score. Thromb Haemost 84:548–552

    CAS  PubMed  Article  Google Scholar 

  22. Donzé J, Le Gal G, Fine MJ, Roy PM, Sanchez O, Verschuren F et al (2008) Prospective validation of the Pulmonary Embolism Severity Index. A clinical prognostic model for pulmonary embolism. Thromb Haemost 100:943–948

    PubMed  Article  Google Scholar 

  23. Jiménez D, Aujesky D, Moores L, Gómez V, Lobo JL, Uresandi F et al (2010) Simplification of the pulmonary embolism severity index for prognostication in patients with acute symptomatic pulmonary embolism. Arch Intern Med 170:1383–1389

    PubMed  Article  Google Scholar 

  24. Jiménez D, Yusen RD, Otero R, Uresandi F, Nauffal D, Laserna E et al (2007) Prognostic models for selecting patients with acute pulmonary embolism for initial outpatient therapy. Chest 132:24–30

    PubMed  Article  Google Scholar 

  25. Bova C, Sanchez O, Prandoni P, Lankeit M, Konstantinides S, Vanni S et al (2014) Identification of intermediate-risk patients with acute symptomatic pulmonary embolism. Eur Respir J 44:694–703

    PubMed  Article  Google Scholar 

  26. Fernández C, Bova C, Sanchez O, Prandoni P, Lankeit M, Konstantinides S et al (2015) Validation of a model for identification of patients at intermediate to high risk for complications associated with acute symptomatic pulmonary embolism. Chest 148:211–218

    PubMed  Article  Google Scholar 

  27. Bova C, Vanni S, Prandoni P, Morello F, Dentali F, Bernardi E et al (2018) Bova Score Validation Study Investigators. A prospective validation of the Bova score in normotensive patients with acute pulmonary embolism. Thromb Res 165:107–111

    CAS  PubMed  Article  Google Scholar 

  28. Dellas C, Tschepe M, Seeber V, Zwiener I, Kuhnert K, Schäfer K et al (2014) A novel H-FABP assay and a fast prognostic score for risk assessment of normotensive pulmonary embolism. Thromb Haemost 111:996–1003

    CAS  PubMed  Article  Google Scholar 

  29. Hobohm L, Becattini C, Konstantinides SV, Casazza F, Lankeit M (2020) Validation of a fast prognostic score for risk stratification of normotensive patients with acute pulmonary embolism. Clin Res Cardiol 109:1008–1017

    PubMed  PubMed Central  Article  Google Scholar 

  30. Kabrhel C, Rosovsky R, Channick R, Jaff MR, Weinberg I, Sundt T et al (2016) A multidisciplinary pulmonary embolism response team: initial 30-month experience with a novel approach to delivery of care to patients with submassive and massive pulmonary embolism. Chest 150:384–393

    PubMed  Article  Google Scholar 

  31. Zern EK, Young MN, Rosenfield K, Kabrhel C (2017) A pulmonary embolism response team: initial experiences and future directions. Expert Rev Cardiovasc Ther 15:481–489

    CAS  PubMed  Article  Google Scholar 

  32. Rivera-Lebron B, McDaniel M, Ahrar K, Alrifai A, Dudzinski DM, Fanola C, et al (2019) PERT Consortium. Diagnosis, treatment and follow up of acute pulmonary embolism: consensus practice from the PERT consortium. Clin Appl Thromb Hemost 25: 1076029619853037.

  33. Carson JL, Kelley MA, Duff A, Weg JG, Fulkerson WJ, Palevsky HI et al (1992) The clinical course of pulmonary embolism. N Engl J Med 326:1240–1245

    CAS  PubMed  Article  Google Scholar 

  34. Key NS, Khorana AA, Kuderer NM, Bohlke K, Lee AYY, Arcelus JI et al (2020) Venous thromboembolism prophylaxis and treatment in patients with cancer: ASCO Clinical Practice Guideline Update. J Clin Oncol 38:496–520

    PubMed  Article  Google Scholar 

  35. Lee AY, Peterson EA (2013) Treatment of cancer-associated thrombosis. Blood 122:2310–2317

    CAS  PubMed  Article  Google Scholar 

  36. Kline JA, Roy PM, Than MP, Hernandez J, Courtney DM, Jones AE et al (2012) Derivation and validation of a multivariate model to predict mortality from pulmonary embolism with cancer: The POMPE-C tool. Thromb Res 129:e194–e199

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. den Exter PL, Gómez V, Jiménez D, Trujillo-Santos J, Muriel A, Huisman MV et al (2013) A clinical prognostic model for the identification of low-risk patients with acute symptomatic pulmonary embolism and active cancer. Chest 143:138–145

    Article  Google Scholar 

  38. Font C, Carmona-Bayonas A, Beato C, Reig Ò, Sáez A, Jiménez-Fonseca P et al (2017) Clinical features and short-term outcomes of cancer patients with suspected and unsuspected pulmonary embolism: the EPIPHANY study. Eur Respir J 49:1600282

    PubMed  Article  Google Scholar 

  39. Posch F, Ay C (2017) Symptoms, signs, suspicion and setting: a PESI score for cancer-associated pulmonary embolism? Eur Respir J 49:1602225

    PubMed  Article  Google Scholar 

  40. Carmona-Bayonas A, Jiménez-Fonseca P, Font C, Fenoy F, Otero R, Beato C et al (2017) Predicting serious complications in patients with cancer and pulmonary embolism using decision tree modelling: the EPIPHANY Index. Br J Cancer 116:994–1001

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. Ahn S, Cooksley T, Banala S, Buffardi L, Rice TW (2018) Validation of the EPIPHANY index for predicting risk of serious complications in cancer patients with incidental pulmonary embolism. Support Care Cancer 26:3601–3607

    PubMed  Article  Google Scholar 

  42. Meyer HJ, Wienke A, Surov A (2021) Incidental pulmonary embolism in oncologic patients-a systematic review and meta-analysis. Support Care Cancer 29:1293–1302

    PubMed  Article  Google Scholar 

  43. Font C, Farrús B, Vidal L, Caralt TM, Visa L, Mellado B et al (2011) Incidental versus symptomatic venous thrombosis in cancer: a prospective observational study of 340 consecutive patients. Ann Oncol 22:2101–2106

    CAS  PubMed  Article  Google Scholar 

  44. Di Nisio M, Ferrante N, De Tursi M, Iacobelli S, Cuccurullo F, Büller HR et al (2010) Incidental venous thromboembolism in ambulatory cancer patients receiving chemotherapy. Thromb Haemost 104:1049–1054

    PubMed  Article  Google Scholar 

  45. van der Hulle T, den Exter PL, Planquette B, Meyer G, Soler S, Monreal M et al (2016) Risk of recurrent venous thromboembolism and major hemorrhage in cancer-associated incidental pulmonary embolism among treated and untreated patients: a pooled analysis of 926 patients. J Thromb Haemost 14:105–113

    PubMed  Article  Google Scholar 

  46. Kraaijpoel N, Bleker SM, Meyer G, Mahé I, Muñoz A, Bertoletti L et al (2019) Treatment and long-term clinical outcomes of incidental pulmonary embolism in patients with cancer: an international prospective cohort study. J Clin Oncol 37:1713–1720

    CAS  PubMed  Article  Google Scholar 

  47. Peris M, López-Nuñez JJ, Maestre A, Jimenez D, Muriel A, Bikdeli B et al (2021) Clinical characteristics and 3-month outcomes in cancer patients with incidental versus clinically suspected and confirmed pulmonary embolism. Eur Respir J 58:2002723

    CAS  PubMed  Article  Google Scholar 

  48. Di Nisio M, Lee AY, Carrier M, Liebman HA, Khorana AA (2015) Subcommittee on haemostasis and malignancy. Diagnosis and treatment of incidental venous thromboembolism in cancer patients: guidance from the SSC of the ISTH. J Thromb Haemost 13:880–883

    PubMed  Article  Google Scholar 

  49. Farge D, Frere C, Connors JM, Ay C, Khorana AA, Munoz A et al (2019) International Initiative on Thrombosis and Cancer (ITAC) advisory panel. 2019 international clinical practice guidelines for the treatment and prophylaxis of venous thromboembolism in patients with cancer. Lancet Oncol 20:e566–e581

    PubMed  Article  Google Scholar 

  50. Lyman GH, Carrier M, Ay C, Di Nisio M, Hicks LK, Khorana AA et al (2021) American Society of Hematology 2021 guidelines for management of venous thromboembolism: prevention and treatment in patients with cancer. Blood Adv 5:927–974

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. Stevens SM, Woller SC, Baumann Kreuziger L, Bounameaux H, Doerschug K, Geersing GJ et al (2021) Antithrombotic therapy for VTE disease: second update of the CHEST Guideline and Expert Panel Report - Executive Summary. Chest S0012–3692(21):01507–01515

    Google Scholar 

  52. Caiano L, Carrier M, Marshall A, Young AM, Ageno W, Delluc A et al (2021) Outcomes among patients with cancer and incidental or symptomatic venous thromboembolism: a systematic review and meta-analysis. J Thromb Haemost 19:2468–2479

    PubMed  Article  Google Scholar 

  53. Aujesky D, Roy PM, Verschuren F, Righini M, Osterwalder J, Egloff M et al (2011) Outpatient versus inpatient treatment for patients with acute pulmonary embolism: an international, open-label, randomised, non-inferiority trial. Lancet 378:41–48

    PubMed  Article  Google Scholar 

  54. Otero R, Uresandi F, Jiménez D, Cabezudo MA, Oribe M, Nauffal D et al (2010) Home treatment in pulmonary embolism. Thromb Res 126:e1–e5

    CAS  PubMed  Article  Google Scholar 

  55. Peacock FW, Coleman CI, Diercks DB, Francis S, Kabrhel C, Keay C et al (2018) Emergency Department Discharge of Pulmonary Embolus Patients. Acad Emerg Med 25:995–1003

    Article  Google Scholar 

  56. Roy PM, Penaloza A, Hugli O, Klok FA, Arnoux A, Elias A et al (2021) HOME-PE Study Group. Triaging acute pulmonary embolism for home treatment by Hestia or simplified PESI criteria: the HOME-PE randomized trial. Eur Heart J 42:3146–3157

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. Zondag W, Mos IC, Creemers-Schild D, Hoogerbrugge AD, Dekkers OM, Dolsma J et al (2011) Outpatient treatment in patients with acute pulmonary embolism: the Hestia Study. J Thromb Haemost 9:1500–1507

    CAS  PubMed  Article  Google Scholar 

  58. Howard LSGE, Barden S, Condliffe R, Connolly V, Davies CWH, Donaldson J, et al (2018) British Thoracic Society Guideline for the initial outpatient management of pulmonary embolism (PE). Thorax 73 (Suppl 2): ii1-ii29.

  59. Peacock WF, Singer AJ (2019) Reducing the hospital burden associated with the treatment of pulmonary embolism. J Thromb Haemost 17:720–736

    PubMed  PubMed Central  Article  Google Scholar 

  60. Westafer LM, Shieh MS, Pekow PS, Stefan MS, Lindenauer PK (2021) Outpatient management of patients following diagnosis of acute pulmonary embolism. Acad Emerg Med 28:336–345

    PubMed  Article  Google Scholar 

  61. Siragusa S, Arcara C, Malato A, Anastasio R, Valerio MR, Fulfaro F, et al (2005) Home therapy for deep vein thrombosis and pulmonary embolism in cancer patients. Ann Oncol 16 Suppl 4: iv136-iv139.

  62. Ageno W, Grimwood R, Limbiati S, Dentali F, Steidl L, Wells PS (2005) Home-treatment of deep vein thrombosis in patients with cancer. Haematologica 90:220–224

    PubMed  Google Scholar 

  63. Font C, Carmona-Bayonas A, Fernández-Martinez A, Beato C, Vargas A, Gascon P et al (2014) Outpatient management of pulmonary embolism in cancer: data on a prospective cohort of 138 consecutive patients. J Natl Compr Canc Netw 12:365–373

    PubMed  Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Consortia

Contributions

All the authors have contributed to the development of the manuscript and approved the last version.

Corresponding author

Correspondence to Carme Font.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

All the co-authors would accept the publication of the manuscript.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Muñoz-Guglielmetti, D., Cooksley, T., Ahn, S. et al. Risk stratification for clinical severity of pulmonary embolism in patients with cancer: a narrative review and MASCC clinical guidance for daily care. Support Care Cancer 30, 8527–8538 (2022). https://doi.org/10.1007/s00520-022-07131-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00520-022-07131-1

Keywords

  • Cancer-associated venous thromboembolism
  • Acute pulmonary embolism
  • Unsuspected pulmonary embolism
  • Supportive care oncology