Relapsed small cell lung cancer: Treatment options and latest developments

Therapeutic Advances in Medical Oncology

Volumn 6, Issue 2, 2014, Pages 69-82

  Asai, Nobuhiro ^a   Ohkuni, Yoshihiro ^b   Kaneko, Norihiro ^b   Yamaguchi, Etsuro ^a   Kubo, Akihito ^a  

^a AICHI MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KAMEDA MEDICAL CENTER   (Japan)

Author keywords

chemotherapy; refractory relapse; sensitive relapse; small cell lung cancer

Indexed keywords

AMRUBICIN; CYTOTOXIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; ETOPOSIDE; GEMCITABINE; IFOSFAMIDE; IRINOTECAN; PEMETREXED; TOPOTECAN;

ANTINEOPLASTIC ACTIVITY; CANCER CHEMOTHERAPY; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER PATIENT; CANCER RECURRENCE; CANCER SURVIVAL; DRUG EFFICACY; HUMAN; LUNG SMALL CELL CANCER; MOLECULARLY TARGETED THERAPY; MONOTHERAPY; OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW;

EID: 84899075856     PISSN: 17588340     EISSN: 17588359     Source Type: Journal    
DOI: 10.1177/1758834013517413     Document Type: Review

References (86)

1. Abrams T. Lee L. Murray L. Pryer N. Cherrington J. (2003) SU 11248 inhibits KIT and platelet-derived growth factor receptor beta in preclinical models of human small cell lung cancer. Mol Cancer Ther 2: 471–478.
2. Allen J. Moon J. Gadgeel S. Kelly K. Mack P. Saba H. et al. (2012) SWOG 0802: a randomized phase II trial of weekly topotecan with and without AVE 0005 (aflibercept) in patients with platinum-treated extensive-stage small cell lung cancer (E-SCLC). 2012 ASCO Annual Meeting. J Clin Oncol 30(Suppl.): abstract 7005.
3. Ando M. Kobayashi K. Yoshimura A. Kurimoto F. Seike M. Nara M. et al. (2004) Weekly administration of irinotecan (CPT-11) plus cisplatin for refractory or relapsed small cell lung cancer. Lung Cancer 44: 121–127.
4. Ardizzoni A. (2004) Topotecan in the treatment of recurrent small cell lung cancer: an update. Oncologist 9(Suppl. 6): 4–13.
5. Ardizzoni A. Antonelli G. Ricci S. Frasci G. Rinaldi M. Boni L. et al. (2000) Ambamustine in the second-line treatment of patients with small-cell lung cancer: a phase II Fonicap study. Am J Clin Oncol 23: 22–25.
6. Asai N. Ohkuni Y. Matsuda M. Kaneko N. (2013) Small-cell lung cancer with epidermal growth factor receptor mutation: case report and review of literature. Indian J Cancer in press.
7. Asai N. Ohkuni Y. Matsunuma R. Nakashima K. Iwasaki T. Kaneko N. (2012) Efficacy and safety of amrubicin for the elderly patients with refractory relapsed small cell lung cancer as third-line chemotherapy. J Cancer Res Ther 2: 266–271.
8. Blackhall F. Shepherd F. (2007) Small cell lung cancer and targeted therapies. Curr Opin Oncol 19: 103–108.
9. Chen J. Jiang R. Garces Y. Jatoi A. Stoddard S. Sun Z. et al. (2010) Prognostic factors for limited-stage small cell lung cancer: a study of 284 patients. Lung Cancer 67: 221–226.
10. Eckardt J. Bentsion D. Lipatov O. Polyakov I. Mackintosh F. Karlin D. et al. (2009) Phase II study of picoplatin as second-line therapy for patients with small-cell lung cancer. J Clin Oncol 27: 2046–2051.
11. Eckardt J. von Pawel J. Pujol J. Papai Z. Quoix E. Ardizzoni A. et al. (2007) Phase III study of oral compared with intravenous topotecan as second-line therapy in small-cell lung cancer. J Clin Oncol 25: 2086–2092.
12. Eisen T. Thatcher N. Leyvraz S. Miller W. Jr Couture F. Lorigan P. et al. (2009) Phase II study of weekly plitidepsin as second-line therapy for small cell lung cancer. Lung Cancer 64: 60–65.
13. Ettinger D. Jotte R. Lorigan P. Gupta V. Garbo L. Alemany C. et al. (2010) Phase II study of amrubicin as second-line therapy in patients with platinum-refractory small-cell lung cancer. J Clin Oncol 28: 2598–2603.
14. Evans W. Feld R. Osoba D. Shepherd F. Dill J. Deboer G. (1984) VP-16 alone and in combination with cisplatin in previously treated patients with small cell lung cancer. Cancer 53: 1461–1466.
15. Faylona E. Loehrer P. Ansari R. Sandler A. Gonin R. Einhorn L. (1995) Phase II study of daily oral etoposide plus ifosfamide plus cisplatin for previously treated recurrent small-cell lung cancer: a Hoosier oncology group trial. J Clin Oncol 13: 1209–1214.
16. Figoli F. Veronesi A. Ardizzoni A. Canobbio L. Bruschi G. Mazza F. et al. (1988) Cisplatin and etoposide as second-line chemotherapy in patients with small cell lung cancer. Cancer Invest 6: 1–5.
17. Gandhi L. Heist R. Lucca J. Temel J. Fidias P. Morse L. et al. (2012) A phase II trial of pazopanib in relapsed / refractory small cell lung cancer (SCLC). 2012 ASCO Annual Meeting. J Clin Oncol 30(Suppl.): abstract 7099.
18. Giaccone G. Ferrati P. Donaldo M. Testore F. Calciati A. (1987) Reinduction chemotherapy in small cell lung cancer. Eur J Cancer Clin Oncol 23: 1697–1699.
19. Glisson B. (2003) Recurrent small cell lung cancer: update. Semin Oncol 30: 72–78.
20. Goto K. Sekine I. Nishiwaki Y. Kakinuma R. Kubota K. Matsumoto T. et al. (2004) Multi-institutional phase II trial of irinotecan, cisplatin, and etoposide for sensitive relapsed small-cell lung cancer. Br J Cancer 91: 659–665.
21. Govindan R. Page N. Morgensztern D. Read W. Tierney R. Vlahiotis A. et al. (2006) Changing epidemiology of small-cell lung cancer in the United States over the last 30 years: analysis of the surveillance, epidemiologic, and end results database. J Clin Oncol 24: 4539–4544.
22. Groen H. Fokkema E. Biesma B. Kwa B. van Putten J. Postmus P. et al. (1999) Paclitaxel and carboplatin in the treatment of small-cell lung cancer patients resistant to cyclophosphamide, doxorubicin, and etoposide: a non-cross-resistant schedule. J Clin Oncol 17: 927–932.
23. Grønberg B. Bremnes R. Aasebø U. Brunsvig P. Fløtten O. Amundsen T. et al. (2009) A prospective phase II study: high-dose pemetrexed as second-line chemotherapy in small-cell lung cancer. Lung Cancer 63: 88–93.
24. Han J. Kim H. Lim K. Han J. Lee Y. Kwak M. et al. (2013) A phase II study of sunitinib in patients with relapsed or refractory small cell lung cancer. Lung Cancer 79: 137–142.
25. Hanada M. Mizuno S. Fukushima A. Saito Y. Noguchi T. Yamaoka T. (1998) A new anticancer agent amrubicin induces cell growth inhibition by stabilizing topoisomerase II-DNA complex. Jpn J Cancer Res 89: 1229–1238.
26. Hanna N. Shepherd F. Fossella F. Pereira J. de Marinis F. von Pawel J. et al. (2004) Randomized phase III trial of pemetrexed versus docetaxel in patients with non-small cell lung cancer previously treated with chemotherapy. J Clin Oncol 22: 1589.
27. Hirose T. Horichi N. Ohmori T. Ogura K. Hosaka T. Ando K. et al. (2003) Phase II study of irinotecan and carboplatin in patients with the refractory or relapsed small cell lung cancer. Lung Cancer 40: 333–338.
28. Hoang T. Kim K. Jaslowski A. Koch P. Beatty P. McGovern J. et al. (2003) Phase II study of second-line gemcitabine in sensitive or refractory small cell lung cancer. Lung Cancer 42: 97–102.
29. Ichiki M. Gohara R. Rikimaru T. Kitajima T. Fujiki R. Shimada A. et al. (2002) Combination chemotherapy with irinotecan and ifosfamide as second-line treatment of refractory or sensitive relapsed small cell lung cancer: a phase II study. Chemotherapy 49: 200–205.
30. Igawa S. Yamamoto N. Ueda S. Ono A. Nakamura Y. Tsuya A. et al. (2007) Evaluation of the recommended dose and efficacy of amrubicin as second- and third-line chemotherapy for small cell lung cancer. J Thorac Oncol 2: 741–744.
31. Inoue A. Sugawara S. Yamazaki K. Maemondo M. Suzuki T. Gomi K. et al. (2008) Randomized phase II trial comparing amrubicin with topotecan in patients with previously treated small-cell lung cancer: North Japan Lung Cancer Study Group Trial 0402. J Clin Oncol 26: 5401–5406.
32. Ioannou M. Papamichali R. Kouvaras E. Mylonis I. Vageli D. Kerenidou T. et al. (2009) Hypoxia inducible factor-1 alpha-1 and vascular endothelial growth factor in biopsies of small cell carcinoma. Lung 187: 321–329.
33. Jalal S. Ansari R. Govindan R. Bhatia S. Bruetman D. Fisher W. et al. (2009) Pemetrexed in second line and beyond small cell lung cancer: a Hoosier Oncology Group phase II study. J Thorac Oncol 4: 93–96.
34. Jassem J. Ramlau R. Santoro A. Schuette W. Chemaissani A. Hong S. et al. (2008) Phase III trial of pemetrexed plus best supportive care compared with best supportive care in previously treated patients with advanced malignant pleural mesothelioma. J Clin Oncol 26: 1698.
35. Johnson D. (1997) Small cell lung cancer in the elderly patient. Semin Oncol 24: 484–491.
36. Jotte R. Conkling P. Reynolds C. Galsky M. Klein L. Fitzgibbons J. et al. (2011 a) Randomized phase II trial of single-agent amrubicin or topotecan as second-line treatment in patients with small-cell lung cancer sensitive to first-line platinum-based chemotherapy. J Clin Oncol 29: 287–293.
37. Jotte R. von Pawel J. Spigel D. Socinski M. O'Brien M. Paschold E. et al. (2011 b) Randomized phase III trial of amrubicin versus topotecan as second-line treatment for small cell lung cancer. 2011 ASCO Annual Meeting. J Clin Oncol 29(Suppl.): abstract 7000.
38. Kaira K. Sunaga N. Tomizawa Y. Yanagitani N. Shimizu K. Imai H. et al. (2010) A phase II study of amrubicin, a synthetic 9-aminoanthracycline, in patients with previously treated lung cancer. Lung Cancer 69: 99–104.
39. Kakolyris S. Mavroudis D. Tsavaris N. Souglakos J. Tsiafaki P. Kalbakis K. et al. (2001) Paclitaxel in combination with carboplatin as salvage treatment in refractory small-cell lung cancer (SCLC): a multicenter phase II study. Ann Oncol 12: 193–197.
40. Kato T. Nokihara H. Ohe Y. Yamamoto N. Sekine I. Kunitoh H. et al. (2006) Phase II trial amrubicin in patients with previously treated small cell lung cancer (SCLC). 2006 ASCO Meeting. J Clin Oncol 24(Suppl.): abstract 7061.
41. Kim Y. Goto K. Nishiwaki Y. Kubota K. Omatsu H. Tamura T. et al. (2006) Phase II study of weekly cisplatin, etoposide, irinotecan (PE/CPT) for refractory relapsed small cell lung cancer (SCLC). 2006 ASCO Meeting. J Clin Oncol 24(Suppl): abstract 7088.
42. Kim Y. Mishima M. (2011) Second-line chemotherapy for small-cell lung cancer. Cancer Treat Rev 37: 143–150.
43. Kimura H. Yamaguchi Y. (1997) A phase III randomized study of interleukin-2 lymphokine-activated killer cell immunotherapy combined with chemotherapy or radiotherapy after curative or noncurative resection of primary lung carcinoma. Cancer 80: 42–49.
44. Kono K. Takahashi A. Ichihara F. Amemiya H. Iizuka H. Fujii H. et al. (2002) Prognostic significance of adoptive immunotherapy with tumor-associated lymphocytes in patients with advanced gastric cancer: a randomized trial. Clin Cancer Res 8: 1767–1771.
45. Kosmas C. Tsavaris N. Malamos N. Vadiaka M. Koufos C. (2001) Phase II study of paclitaxel, ifosfamide, and cisplatin as second-line treatment in relapsed small-cell lung cancer. J Clin Oncol 19: 119–126.
46. Krystal G. Hines S. Organ C. (1996) Autocrine growth of small cell lung cancer mediated by coexpression of c-kit and stem cell factor. Cancer Res 56: 370–376.
47. Kubota K. Nishiwaki Y. Kakinuma R. Hojo F. Matsumoto T. Ohmatsu H. et al. (1997) Dose-intensive weekly chemotherapy for treatment of relapsed small-cell lung cancer. J Clin Oncol 15: 292–296.
48. Lee P. Alvarez R. Melichar B. Adenis A. Bennouna J. Schusterbauer C. et al. (2012) Phase I / II study of the investigational aurora A kinase (AAK) inhibitor MLN 8237 (alisertib) in patients (pts) with non-small cell lung cancer (NSCLC), small cell lung cancer (SCLC), breast (BrC), head / neck cancer (H&N), and gastroesophageal (GE) adenocarcinoma: preliminary phase II results. 2012 ASCO Annual Meeting. J Clin Oncol 30(Suppl.): abstract 3010.
49. Lucchi M. Mussi A. Fontanini G. Faviana P. Ribechini A. Angeletti C. (2002) Small cell lung carcinoma (SCLC): the angiogenic phenomenon. Eur J Cardiothorac Surg 21: 1105–1110.
50. Maalouf G. Rodier J. Faivre S. Raymond E. (2007) Could we expect to improve survival in small cell lung cancer. Lung Cancer 57(Suppl.): S30–S34.
51. Maemondo M. Inoue A. Kobayashi K. Sugawara S. Oizumi S. Isobe H. et al. (2010) Gefitinib or chemotherapy for mom-small cell lung cancer with mutated EGFR. N Eng J Med 362: 2380–2388.
52. Masuda N. Fukuoka M. Kusunoki Y. Matsui K. Takifuji N. Kudoh S. et al. (1992) CPT-11: a new derivative of campto thecin for the treatment of refractory or relapsed small-cell lung cancer. J Clin Oncol 10: 1225–1229.
53. Masuda N. Matsui K. Negoro S. Takifuji N. Takeda K. Yana T. et al. (1998) Combination of irinotecan and etoposide for treatment of refractory relapsed small-cell lung cancer. J Clin Oncol 16: 3329–3334.
54. Noda K. Nishiwaki Y. Kawahara M. Negoro S. Sugiura T. Yokoyama A. et al. (2002) Irinotecan plus cisplatin compared with etoposide plus cisplatin for extensive small-cell lung cancer. N Engl J Med 346: 85–91.
55. Noda T. Watanabe T. Kohda A. Hosokawa S. Suzuki T. (1998) Chronic effects of a novel synthetic anthracycline derivative (SM-5887) on normal heart and doxorubicin-induced cardiomyopathy in beagle dogs. Invest New Drugs 16: 121–128.
56. Noguchi T. Ichii S. Morisada S. Yamaoka T. Yanagi Y. (1998 a) In vivo efficacy and tumorselective metabolism of amrubicin to its active metabolite. Jpn J Cancer Res 89: 1055–1060.
57. Noguchi T. Ichii S. Morisada S. Yamaoka T. Yanagi Y. (1998 b) Tumor-selective distribution of an active metabolite of the 9-aminoanthracycline amrubicin. Jpn J Cancer Res 89: 1061–1066.
58. O'Brien M. Ciuleanu T. Tsekov H. Shparyk Y. Cuceviá B. Juhasz G. et al. (2006) Phase III trial comparing supportive care alone with supportive care with oral topotecan in patients with relapsed small-cell lung cancer. J Clin Oncol 24: 5441–5447.
59. Ohe Y. Nakagawa K. Fujiwara Y. Sasaki Y. Minato K. Bungo M. et al. (1989) In vitro evaluation of the new anticancer agents KT6149, MX-2, SM5887, menogaril, and liblomycin using cisplatin- or adriamycin-resistant human cancer cell lines. Cancer Coooperative Group. Eur J Cancer 49: 4098–4102.
60. Onoda S. Masuda N. Seto T. Eguchi K. Takiguchi Y. Isobe H. et al. (2006) Phase II trial of amrubicin in patients with previously or relapsed small-cell lung cancer: Thoracic Oncology Research Group Study 0301. J Clin Oncol 24: 5448–5453.
61. Pallis A. Agelidou A. Agelaki S. Varthalitis I. Pavlakou G. Gerogianni A. et al. (2009) A multicenter randomized phase II study of the irinotecan / gemcitabine doublet versus irinotecan monotherapy in previously treated patients with extensive stage small-cell lung cancer. Lung Cancer 65: 187–191.
62. Park S. Ahn M. Ahn J. Lee J. Hong Y. Park B. et al. (2007) Combination chemotherapy with paclitaxel and ifosfamide as the third-line regimen in patients with heavily pretreated small cell lung cancer. Lung Cancer 58: 116–122.
63. Postmus P. Berendsen H. van Zandwijk N. Splinter T. Burghouts J. Bakker W. et al. (1987) Retreatment with the induction regimen in small cell lung cancer relapsing after an initial response to short term chemotherapy. Eur J Cancer Clin Oncol 23: 1409–1411.
64. Postmus P. Smit E. Berendsen H. Haaxma-Reiche H. (1992) Second-line carboplatin-based chemotherapy for small cell lung cancer: the Groningen experience. Semin Oncol 19: 17–23.
65. Postmus P. Smit E. Kirkpatrick A. Splinter T. (1993) Testing the possible non-cross resistance of two equipotent combination chemotherapy regimens against small-cell lung cancer: a phase II study of the EORTC lung cancer cooperative group. Eur J Cancer 29A: 204–207.
66. Rosell R. Moran T. Queralt C. Porta R. Cardenal F. Camps C. et al. (2009) Screening for epidermal growth factor receptor mutations in lung cancer. N Eng J Med 361: 958–967.
67. Rosti G. Bevilacqua G. Bidoli P. Portalone L. Santo A. Genestreti G. (2006) Small cell lung cancer. Ann Oncol 17(Suppl. 2): ii5–ii10.
68. Salven P. Ruotsalainen T. Mattson K. Joensuu H. (1998) High pre-treatment serum level of vascular endothelial growth factor (VEGF) is associated with poor outcome in small-cell lung cancer. Int J Cancer 79: 144–146.
69. Samantas E. Kalofonos H. Linardou H. Nicolaides C. Mylonakis N. Fountzilas G. et al. (2000) Phase II study of pegylated liposomal doxorubicin: inactive in recurrent small-cell lung cancer. A Hellenic Cooperative Oncology Group Study. Ann Oncol 11: 1395–1397.
70. Schmittel A. Knödler M. Hortig P. Schulze K. Thiel E. Keilholz U. (2007) Phase II trial of second-line bendamustine chemotherapy in relapsed small cell lung cancer patients. Lung Cancer 55: 109–113.
71. Schuette W. Nagel S. Juergens S. Bork I. Wollschlaeger B. Schaedlich S. et al. (2005) Phase II trial of gemcitabine / irinotecan in refractory or relapsed small-cell lung cancer. Clin Lung Cancer 7: 133–137.
72. Shigematsu H. Gazdar A. (2006) Somatic mutations of epidermal growth factor receptor signaling pathway in lung cancers. Int J Cancer 118: 257–262.
73. Shih C. Chen V. Gossetti L. Gates S. MacKellar W. Habeck L. et al. (1997) LY231514, a pyrrolo [2,3-d] pyrimidine-based antifolate that inhibits multiple folate-requiring enzymes. Cancer Res 57: 1116–1123.
74. Smit E. Fokkema E. Biesma B. Groen H. Snoek W. Postmus P. (1998) A phase II study of paclitaxel in heavily pretreated patients with small-cell lung cancer. Br J Cancer 77: 347–351.
75. Takayama T. Sekine T. Makuuchi M. Yamasaki S. Kosuge T. Yamamoto J. et al. (2000) Adoptive immunotherapy to lower postsurgical recurrence rates of hepatocellular carcinoma: a randomised trial. Lancet 356: 802–807.
76. Tanaka F. Wada H. Fukui Y. Fukushima M. (2011). Thymidylate synthase (TS) gene expression in primary lung cancer patients: a large-scale study in Japanese population. Ann Oncol 22: 1791–1797.
77. Tanno S. Ohsaki Y. Nakanishi K. Toyoshima E. Kikuchi K. (2004) Human small cell lung cancer cells express functional VEGF receptors, VEGFR-2 and VEGFR-3. Lung Cancer 46: 11–19.
78. Tas F. Duranyildiz D. Oguz H. Camlica H. Yasasever V. Topuz E. (2006) Serum vascular endothelial growth factor (VEGF) and interleukin-8 (IL-8) levels in small cell lung cancer. Cancer Invest 24: 492–496.
79. Tatematsu A. Shimizu J. Murakami Y. Horio Y. Nakamura S. Hida T. et al. (2008) Epidermal growth factor receptor mutations in small cell lung cancer. Clin Cancer Res 14: 6092–6096.
80. Ustuner Z. Saip P. Yasasever V. Vural B. Yazar A. Bal C. et al. (2008) Prognostic and predictive value of vascular endothelial growth factor and its soluble receptors, VEGFR-1 and VEGFR-2 levels in the sera of small cell lung cancer patients. Med Oncol 25: 394–399.
81. von Pawel J. Ardizzoni A. Thatcher N. (2003) The relationship between treatment-free interval (TFI) and outcomes to therapy in patients with relapsed small cell lung cancer (SCLC): a review of 631 patients treated with iv topotecan in 6 studies. Lung Cancer 41(Suppl. 2): S235.
82. von Pawel J. Gatzemeier U. Pujol J. Moreau L. Bildat S. Ranson M. et al. (2001) Phase II comparator study of oral versus intravenous topotecan in patients with chemosensitive small-cell lung cancer. J Clin Oncol 19: 1743–1749.
83. von Pawel J. Schiller J. Shepherd F. Fields S. Kleisbauer J. Chrysson N. et al. (1999) Topotecan versus cyclophosphamide, doxorubicin, and vincristine for the treatment of recurrent small-cell lung cancer. J Clin Oncol 17: 658–667.
84. Wolff S. Birch R. Sarma P. Greco F. (1986) Randomized dose–response evaluation of etoposide in small cell carcinoma of the lung: a Southeastern Cancer Study Group Trial. Cancer Treat Rep 70: 583–587.
85. Yana T. Negoro S. Takada M. Yokota S. Takada Y. Sugiura T. et al. (2007) Phase II study of amrubicin in previously untreated patients with extensive-disease small cell lung cancer: West Japan Thoracic Oncology Group (WJTOG) study. Invest New Drugs 25: 253–258.
86. Zhan P. Wang J. Lv X. Wang Q. Qiu L. Lin X. et al. (2009) Prognostic value of vascular endothelial growth factor expression in patients with lung cancer: a systematic review with meta-analysis. J Thorac Oncol 4: 1094–1103.