Research progress of hyperprogressive disease in malignant tumors treated with immune checkpoint inhibitors therapy_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

FENG Lei ¹ , CHENG Hua ² ,  CHEN Liping ¹

1. Department of Biliary Surgery, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;
2. Department of Intensive Care Unit, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

CHEN Liping, Email: 47137417@qq.com

Keywords：

hyperprogressive disease; malignant tumor; immunotherapy; immune checkpoint inhibitor; pseudoprogress

DOI：

10.7507/1007-9424.202101023

Video：

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Objective To review the definition, incidence, risk factors, potential pathogenesis, biomarkers, and choice of follow-up treatment strategies of hyperprogressive disease (HPD).Method Domestic and international literatures were collected to summarize the research progress of HPD in patients with malignant tumors who treated with immune checkpoint inhibitors (ICIs).Results The research types of HPD were scattered, the sample size was limited, the definition standard was different, and there was lack of prospective validation studies. Therefore, the early warning assessment and molecular mechanism of HPD would become the next focus of the study of immunotherapy.Conclusion ICIs can greatly improve the survival time of some patients with advanced malignant tumor, although some patients have HPD during treatment, but the incidence is relatively low.

Citation： FENG Lei, CHENG Hua, CHEN Liping. Research progress of hyperprogressive disease in malignant tumors treated with immune checkpoint inhibitors therapy. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(11): 1516-1523. doi: 10.7507/1007-9424.202101023 Copy

1.	张诗民, 陈元, 褚倩. 免疫检查点抑制剂治疗肿瘤的不良反应及管理策略. 中国肿瘤临床, 2018, 45(12): 609-613.
2.	Salama AK, Moschos SJ. Next steps in immuno-oncology: enhancing antitumor effects through appropriate patient selection and rationally designed combination strategies. Ann Oncol, 2017, 28(1): 57-74.
3.	Champiat S, Dercle L, Ammari S, et al. Hyperprogressive disease is a new pattern of progression in cancer patients treated by anti-PD-1/PD-L1. Clin Cancer Res, 2017, 23(8): 1920-1928.
4.	Chubachi S, Yasuda H, Irie H, et al. A case of non-small cell lung cancer with possible “disease flare” on nivolumab treatment. Case Rep Oncol Med, 2016, 2016: 1075641.
5.	Faure M, Rochigneux P, Olive D, et al. Hyperprogressive disease in anorectal melanoma treated by PD-1 inhibitors. Front Immunol, 2018, 9: 797.
6.	Occhipinti M, Falcone R, Onesti CE, et al. Hyperprogressive disease and early hypereosinophilia after anti-PD-1 treatment: A case report. Drug Saf Case Rep, 2018, 5(1): 12.
7.	Shinozaki T, Iwami E, Ikemura S, et al. A case of pulmonary adenocarcinoma showing rapid progression of peritoneal dissemination after immune checkpoint inhibitor therapy. BMC Cancer, 2018, 18(1): 620.
8.	Yoshida T, Furuta H, Hida T. Risk of tumor flare after nivolumab treatment in patients with irradiated field recurrence. Med Oncol, 2017, 34(3): 34.
9.	Saâda-Bouzid E, Defaucheux C, Karabajakian A, et al. Hyperprogression during anti-PD-1/PD-L1 therapy in patients with recurrent and/or metastatic head and neck squamous cell carcinoma. Ann Oncol, 2017, 28(7): 1605-1611.
10.	Kato S, Goodman A, Walavalkar V, et al. Hyperprogressors after immunotherapy: Analysis of genomic alterations associated with accelerated growth rate. Clin Cancer Res, 2017, 23(15): 4242-4250.
11.	Weiss GJ, Beck J, Braun DP, et al. Tumor cell-free DNA copy number instability predicts therapeutic response to immunotherapy. Clin Cancer Res, 2017, 23(17): 5074-5081.
12.	Ogata T, Satake H, Ogata M, et al. Hyperprogressive disease in the irradiation field after a single dose of nivolumab for gastric cancer: A case report. Case Rep Oncol, 2018, 11(1): 143-150.
13.	Denaro N. Hyperprogression after immunotherapy in HNC: literature review and our experience. Int J Radiol Radiat Oncol, 2018, 4(1): 1-2.
14.	Ferrara R, Mezquita L, Texier M, et al. Hyperprogressive disease in patients with advanced non-small cell lung cancer treated withPD-1/PD-L1 inhibitors or with single-agent chemotherapy. JAMA Oncol, 2018, 4(11): 1543-1552.
15.	Zhang D, Zhang Y, Huang Y, et al. Hyper-progressive disease in a patient with advanced non-small cell lung cancer on immune checkpoint inhibitor therapy: A case report and literature review. Lung Cancer, 2020, 139: 18-21.
16.	Xu Z, Chen L, Zheng L, et al. Hyperprogressive disease in cervical small cell carcinoma treated by immune checkpoint inhibitor. Onco Targets Ther, 2019, 12: 8873-8877.
17.	Yilmaz M, Akovali B. Hyperprogression after nivolumab for melanoma: A case report. J Oncol Pharm Pract, 2020, 26(1): 244-251.
18.	Sama S, Hadfield MJ, Lopetegui Lia N, et al. Hyperprogression in PDL1 expressive, recurrent gastroesophageal-junction adenocarcinoma after pembrolizumab. Cureus, 2019, 11(6): e4862.
19.	Therasse P, Arbuck SG, Eisenhauer EA, et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst, 2000, 92(3): 205-216.
20.	Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer, 2009, 45(2): 228-247.
21.	Singavi AK, Menon S, Kilari D, et al. Predictive biomarkers for hyper-progression (HP) in response to immune checkpoint inhibitors (ICI)-Analysis of somatic alterations (SAs). Ann Oncol, 2017, 28: v405.
22.	Lo Russo G, Moro M, Sommariva M, et al. Antibody-Fc/FcR interaction on macrophages as a mechanism for hyperprogressive disease in non-small cell lung cancer subsequent to PD-1/PD-L1 blockade. Clin Cancer Res, 2019, 25(3): 989-999.
23.	Matos I, Martin-Liberal J, Hierro C, et al. Incidence and clinical implications of a new definition of hyperprogression (HPD) with immune checkpoint inhibitors (ICIs) in patients treated in phase 1 (Ph1) trials. J Clin Oncol, 2018, 36(15_suppl): 3032.
24.	Kanjanapan Y, Day D, Wang L, et al. Hyperprogressive disease in early-phase immunotherapy trials: Clinical predictors and association with immune-related toxicities. Cancer, 2019, 125(8): 1341-1349.
25.	Kim CG, Kim KH, Pyo KH, et al. Hyperprogressive disease during PD-1/PD-L1 blockade in patients with non-small-cell lung cancer. Ann Oncol, 2019, 30(7): 1104-1113.
26.	Hwang I, Park I, Yoon SK, et al. Hyperprogressive disease in patients with urothelial carcinoma or renal cell carcinoma treated with PD-1/PD-L1 inhibitors. Clin Genitourin Cancer, 2020, 18(2): e122-e133.
27.	Petrioli R, Mazzei MA, Giorgi S, et al. Hyperprogressive disease in advanced cancer patients treated with nivolumab: a case series study. Anticancer Drugs, 2020, 31(2): 190-195.
28.	Rittmeyer A, Barlesi F, Waterkamp D, et al. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet, 2017, 389(10066): 255-265.
29.	Yu G, Xie X, Sun D, et al. EGFR mutation L747P led to gefitinib resistance and accelerated liver metastases in a Chinese patient with lung adenocarcinoma. Int J Clin Exp Pathol, 2015, 8(7): 8603-8606.
30.	Sasaki A, Nakamura Y, Mishima S, et al. Predictive factors for hyperprogressive disease during nivolumab as anti-PD1 treatment in patients with advanced gastric cancer. Gastric Cancer, 2019, 22(4): 793-802.
31.	Lee CK, Man J, Lord S, et al. Clinical and molecular characteristics associated with survival among patients treated with checkpoint inhibitors for advanced non-small cell lung carcinoma: A systematic review and meta-analysis. JAMA Oncol, 2018, 4(2): 210-216.
32.	Peng W, Chen JQ, Liu C, et al. Loss of PTEN promotes resistance to T cell-mediated immunotherapy. Cancer Discov, 2016, 6(2): 202-216.
33.	Azuma K, Ota K, Kawahara A, et al. Association of PD-L1 overexpression with activating EGFR mutations in surgically resected nonsmall-cell lung cancer. Ann Oncol, 2014, 25(10): 1935-1940.
34.	Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med, 2008, 359(13): 1367-1380.
35.	Yamada T, Hirai S, Katayama Y, et al. Retrospective efficacy analysis of immune checkpoint inhibitors in patients with EGFR-mutated non-small cell lung cancer. Cancer Med, 2019, 8(4): 1521-1529.
36.	Gettinger S, Horn L, Jackman D, et al. Five-year follow-up of nivolumab in previously treated advanced non-small-cell lung cancer: Results from the CA209-003 study. J Clin Oncol, 2018, 36(17): 1675-1684.
37.	Yoshida H, Kim YH, Ozasa H, et al. Nivolumab in non-small-cell lung cancer with EGFR mutation. Ann Oncol, 2018, 29(3): 777-778.
38.	Borghaei H, Paz-Ares L, Horn L, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med, 2015, 373(17): 1627-1639.
39.	Ferris RL, Blumenschein G, Fayette J, et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med, 2016, 375(19): 1856-1867.
40.	Bellmunt J, de Wit R, Vaughn DJ, et al. Pembrolizumab as second-line therapy for advanced urothelial carcinoma. N Engl J Med, 2017, 376(11): 1015-1026.
41.	Champiat S, Ferrara R, Massard C, et al. Hyperprogressive disease: recognizing a novel pattern to improve patient management. Nat Rev Clin Oncol, 2018, 15(12): 748-762.
42.	Ji RR, Chasalow SD, Wang L, et al. An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol Immunother, 2012, 61(7): 1019-1031.
43.	Harlin H, Meng Y, Peterson AC, et al. Chemokine expression in melanoma metastases associated with CD8⁺ T-cell recruitment. Cancer Res, 2009, 69(7): 3077-3085.
44.	Kirilovsky A, Marliot F, El Sissy C, et al. Rational bases for the use of the immunoscore in routine clinical settings as a prognostic and predictive biomarker in cancer patients. Int Immunol, 2016, 28(8): 373-382.
45.	Kuriyama Y, Kim YH, Nagai H, et al. Disease flare after discontinuation of crizotinib in anaplastic lymphoma kinase-positive lung cancer. Case Rep Oncol, 2013, 6(2): 430-433.
46.	Duan J, Cui L, Zhao X, et al. Use of immunotherapy with programmed cell death 1 vs programmed cell death ligand 1 inhibitors in patients with cancer: A systematic review and meta-analysis. JAMA Oncol, 2020, 6(3): 375-384.
47.	Imafuku K, Hata H, Kitamura S, et al. Ultrasonographic findings can identify ‘pseudoprogression’ under nivolumab therapy. Br J Dermatol, 2017, 177(6): 1726-1731.

1. 张诗民, 陈元, 褚倩. 免疫检查点抑制剂治疗肿瘤的不良反应及管理策略. 中国肿瘤临床, 2018, 45(12): 609-613.
2. Salama AK, Moschos SJ. Next steps in immuno-oncology: enhancing antitumor effects through appropriate patient selection and rationally designed combination strategies. Ann Oncol, 2017, 28(1): 57-74.
3. Champiat S, Dercle L, Ammari S, et al. Hyperprogressive disease is a new pattern of progression in cancer patients treated by anti-PD-1/PD-L1. Clin Cancer Res, 2017, 23(8): 1920-1928.
4. Chubachi S, Yasuda H, Irie H, et al. A case of non-small cell lung cancer with possible “disease flare” on nivolumab treatment. Case Rep Oncol Med, 2016, 2016: 1075641.
5. Faure M, Rochigneux P, Olive D, et al. Hyperprogressive disease in anorectal melanoma treated by PD-1 inhibitors. Front Immunol, 2018, 9: 797.
6. Occhipinti M, Falcone R, Onesti CE, et al. Hyperprogressive disease and early hypereosinophilia after anti-PD-1 treatment: A case report. Drug Saf Case Rep, 2018, 5(1): 12.
7. Shinozaki T, Iwami E, Ikemura S, et al. A case of pulmonary adenocarcinoma showing rapid progression of peritoneal dissemination after immune checkpoint inhibitor therapy. BMC Cancer, 2018, 18(1): 620.
8. Yoshida T, Furuta H, Hida T. Risk of tumor flare after nivolumab treatment in patients with irradiated field recurrence. Med Oncol, 2017, 34(3): 34.
9. Saâda-Bouzid E, Defaucheux C, Karabajakian A, et al. Hyperprogression during anti-PD-1/PD-L1 therapy in patients with recurrent and/or metastatic head and neck squamous cell carcinoma. Ann Oncol, 2017, 28(7): 1605-1611.
10. Kato S, Goodman A, Walavalkar V, et al. Hyperprogressors after immunotherapy: Analysis of genomic alterations associated with accelerated growth rate. Clin Cancer Res, 2017, 23(15): 4242-4250.
11. Weiss GJ, Beck J, Braun DP, et al. Tumor cell-free DNA copy number instability predicts therapeutic response to immunotherapy. Clin Cancer Res, 2017, 23(17): 5074-5081.
12. Ogata T, Satake H, Ogata M, et al. Hyperprogressive disease in the irradiation field after a single dose of nivolumab for gastric cancer: A case report. Case Rep Oncol, 2018, 11(1): 143-150.
13. Denaro N. Hyperprogression after immunotherapy in HNC: literature review and our experience. Int J Radiol Radiat Oncol, 2018, 4(1): 1-2.
14. Ferrara R, Mezquita L, Texier M, et al. Hyperprogressive disease in patients with advanced non-small cell lung cancer treated withPD-1/PD-L1 inhibitors or with single-agent chemotherapy. JAMA Oncol, 2018, 4(11): 1543-1552.
15. Zhang D, Zhang Y, Huang Y, et al. Hyper-progressive disease in a patient with advanced non-small cell lung cancer on immune checkpoint inhibitor therapy: A case report and literature review. Lung Cancer, 2020, 139: 18-21.
16. Xu Z, Chen L, Zheng L, et al. Hyperprogressive disease in cervical small cell carcinoma treated by immune checkpoint inhibitor. Onco Targets Ther, 2019, 12: 8873-8877.
17. Yilmaz M, Akovali B. Hyperprogression after nivolumab for melanoma: A case report. J Oncol Pharm Pract, 2020, 26(1): 244-251.
18. Sama S, Hadfield MJ, Lopetegui Lia N, et al. Hyperprogression in PDL1 expressive, recurrent gastroesophageal-junction adenocarcinoma after pembrolizumab. Cureus, 2019, 11(6): e4862.
19. Therasse P, Arbuck SG, Eisenhauer EA, et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst, 2000, 92(3): 205-216.
20. Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer, 2009, 45(2): 228-247.
21. Singavi AK, Menon S, Kilari D, et al. Predictive biomarkers for hyper-progression (HP) in response to immune checkpoint inhibitors (ICI)-Analysis of somatic alterations (SAs). Ann Oncol, 2017, 28: v405.
22. Lo Russo G, Moro M, Sommariva M, et al. Antibody-Fc/FcR interaction on macrophages as a mechanism for hyperprogressive disease in non-small cell lung cancer subsequent to PD-1/PD-L1 blockade. Clin Cancer Res, 2019, 25(3): 989-999.
23. Matos I, Martin-Liberal J, Hierro C, et al. Incidence and clinical implications of a new definition of hyperprogression (HPD) with immune checkpoint inhibitors (ICIs) in patients treated in phase 1 (Ph1) trials. J Clin Oncol, 2018, 36(15_suppl): 3032.
24. Kanjanapan Y, Day D, Wang L, et al. Hyperprogressive disease in early-phase immunotherapy trials: Clinical predictors and association with immune-related toxicities. Cancer, 2019, 125(8): 1341-1349.
25. Kim CG, Kim KH, Pyo KH, et al. Hyperprogressive disease during PD-1/PD-L1 blockade in patients with non-small-cell lung cancer. Ann Oncol, 2019, 30(7): 1104-1113.
26. Hwang I, Park I, Yoon SK, et al. Hyperprogressive disease in patients with urothelial carcinoma or renal cell carcinoma treated with PD-1/PD-L1 inhibitors. Clin Genitourin Cancer, 2020, 18(2): e122-e133.
27. Petrioli R, Mazzei MA, Giorgi S, et al. Hyperprogressive disease in advanced cancer patients treated with nivolumab: a case series study. Anticancer Drugs, 2020, 31(2): 190-195.
28. Rittmeyer A, Barlesi F, Waterkamp D, et al. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet, 2017, 389(10066): 255-265.
29. Yu G, Xie X, Sun D, et al. EGFR mutation L747P led to gefitinib resistance and accelerated liver metastases in a Chinese patient with lung adenocarcinoma. Int J Clin Exp Pathol, 2015, 8(7): 8603-8606.
30. Sasaki A, Nakamura Y, Mishima S, et al. Predictive factors for hyperprogressive disease during nivolumab as anti-PD1 treatment in patients with advanced gastric cancer. Gastric Cancer, 2019, 22(4): 793-802.
31. Lee CK, Man J, Lord S, et al. Clinical and molecular characteristics associated with survival among patients treated with checkpoint inhibitors for advanced non-small cell lung carcinoma: A systematic review and meta-analysis. JAMA Oncol, 2018, 4(2): 210-216.
32. Peng W, Chen JQ, Liu C, et al. Loss of PTEN promotes resistance to T cell-mediated immunotherapy. Cancer Discov, 2016, 6(2): 202-216.
33. Azuma K, Ota K, Kawahara A, et al. Association of PD-L1 overexpression with activating EGFR mutations in surgically resected nonsmall-cell lung cancer. Ann Oncol, 2014, 25(10): 1935-1940.
34. Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med, 2008, 359(13): 1367-1380.
35. Yamada T, Hirai S, Katayama Y, et al. Retrospective efficacy analysis of immune checkpoint inhibitors in patients with EGFR-mutated non-small cell lung cancer. Cancer Med, 2019, 8(4): 1521-1529.
36. Gettinger S, Horn L, Jackman D, et al. Five-year follow-up of nivolumab in previously treated advanced non-small-cell lung cancer: Results from the CA209-003 study. J Clin Oncol, 2018, 36(17): 1675-1684.
37. Yoshida H, Kim YH, Ozasa H, et al. Nivolumab in non-small-cell lung cancer with EGFR mutation. Ann Oncol, 2018, 29(3): 777-778.
38. Borghaei H, Paz-Ares L, Horn L, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med, 2015, 373(17): 1627-1639.
39. Ferris RL, Blumenschein G, Fayette J, et al. Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med, 2016, 375(19): 1856-1867.
40. Bellmunt J, de Wit R, Vaughn DJ, et al. Pembrolizumab as second-line therapy for advanced urothelial carcinoma. N Engl J Med, 2017, 376(11): 1015-1026.
41. Champiat S, Ferrara R, Massard C, et al. Hyperprogressive disease: recognizing a novel pattern to improve patient management. Nat Rev Clin Oncol, 2018, 15(12): 748-762.
42. Ji RR, Chasalow SD, Wang L, et al. An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol Immunother, 2012, 61(7): 1019-1031.
43. Harlin H, Meng Y, Peterson AC, et al. Chemokine expression in melanoma metastases associated with CD8⁺ T-cell recruitment. Cancer Res, 2009, 69(7): 3077-3085.
44. Kirilovsky A, Marliot F, El Sissy C, et al. Rational bases for the use of the immunoscore in routine clinical settings as a prognostic and predictive biomarker in cancer patients. Int Immunol, 2016, 28(8): 373-382.
45. Kuriyama Y, Kim YH, Nagai H, et al. Disease flare after discontinuation of crizotinib in anaplastic lymphoma kinase-positive lung cancer. Case Rep Oncol, 2013, 6(2): 430-433.
46. Duan J, Cui L, Zhao X, et al. Use of immunotherapy with programmed cell death 1 vs programmed cell death ligand 1 inhibitors in patients with cancer: A systematic review and meta-analysis. JAMA Oncol, 2020, 6(3): 375-384.
47. Imafuku K, Hata H, Kitamura S, et al. Ultrasonographic findings can identify ‘pseudoprogression’ under nivolumab therapy. Br J Dermatol, 2017, 177(6): 1726-1731.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Research progress of hyperprogressive disease in malignant tumors treated with immune checkpoint inhibitors therapy

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