Sarcopenia is an independent prognostic factor in male patients with diffuse large B-cell lymphoma

Annals of Hematology

Volumn 94, Issue 12, 2015, Pages 2043-2053

  Nakamura, Nobuhiko ^a   Hara, Takeshi ^a   Shibata, Yuhei ^a   Matsumoto, Takuro ^a   Nakamura, Hiroshi ^a   Ninomiya, Soranobu ^a   Kito, Yusuke ^a   Kitagawa, Junichi ^a   Kanemura, Nobuhiro ^a   Goto, Naoe ^a   Shiraki, Makoto ^a   Miyazaki, Tatsuhiko ^b   Takeuchi, Tamotsu ^a   Shimizu, Masahito ^a   Tsurumi, Hisashi ^a  

^a GIFU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b GIFU UNIVERSITY HOSPITAL   (Japan)

Author keywords

Diffuse large B cell lymphoma (DLBCL); Sarcopenia; Skeletal muscle index (SMI)

Indexed keywords

ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; BILIRUBIN; CARBOPLATIN; CREATININE; CYCLOPHOSPHAMIDE; DOXORUBICIN; ETOPOSIDE; FLUORODEOXYGLUCOSE F 18; GRANULOCYTE COLONY STIMULATING FACTOR; IFOSFAMIDE; LACTATE DEHYDROGENASE; METHOTREXATE; METHYLPREDNISOLONE; PIRARUBICIN; PREDNISONE; RITUXIMAB; VINCRISTINE; ANTINEOPLASTIC AGENT; MONOCLONAL ANTIBODY; PREDNISOLONE; R-CHOP PROTOCOL;

ABDOMEN; ADULT; AGED; ALKALINE PHOSPHATASE BLOOD LEVEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILIRUBIN BLOOD LEVEL; BONE MARROW BIOPSY; BRAIN; BRAIN INFARCTION; CANCER COMBINATION CHEMOTHERAPY; CANCER PATIENT; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER STAGING; CANCER SURVIVAL; CAUSE OF DEATH; COMPUTER ASSISTED TOMOGRAPHY; CREATININE BLOOD LEVEL; FEMALE; FEVER; FOLLOW UP; HUMAN; INTERNATIONAL PROGNOSTIC INDEX; LACTATE DEHYDROGENASE BLOOD LEVEL; LARGE CELL LYMPHOMA; MAJOR CLINICAL STUDY; MALE; MULTIMODAL CHEMOTHERAPY; MULTIMODALITY CANCER THERAPY; MUSCLE TISSUE; NECK; NIGHT SWEAT; NUCLEAR MAGNETIC RESONANCE IMAGING; OVERALL SURVIVAL; PELVIS; PHYSICAL EXAMINATION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SARCOPENIA; SEPSIS; SKELETAL MUSCLE; THORAX; THORAX RADIOGRAPHY; UNSPECIFIED SIDE EFFECT; WEIGHT REDUCTION; ANALOGS AND DERIVATIVES; CLINICAL TRIAL; COMPUTED TOMOGRAPHY SCANNER; LYMPHOMA, LARGE B-CELL, DIFFUSE; MIDDLE AGED; RADIOGRAPHY; SEXUAL DEVELOPMENT; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CYCLOPHOSPHAMIDE; DOXORUBICIN; FEMALE; HUMANS; LYMPHOMA, LARGE B-CELL, DIFFUSE; MALE; MIDDLE AGED; MUSCLE, SKELETAL; PREDNISOLONE; PREDNISONE; RETROSPECTIVE STUDIES; SARCOPENIA; SEX CHARACTERISTICS; TOMOGRAPHY SCANNERS, X-RAY COMPUTED; VINCRISTINE;

EID: 84944162338     PISSN: 09395555     EISSN: 14320584     Source Type: Journal    
DOI: 10.1007/s00277-015-2499-4     Document Type: Article

References (55)

1. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman JW (2008) WHO classification of tumours of haematopoietic and lymphoid tissues, 4th edn. IARC, Lyon
2. Coiffier B, Lepage E, Briere J, Herbrecht R, Tilly H, Bouabdallah R, Morel P, Van Den Neste E, Salles G, Gaulard P, Reyes F, Lederlin P, Gisselbrecht C (2002) CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B-cell lymphoma. N Engl J Med 346(4):235–242. doi:10.1056/NEJMoa011795
3. Sehn LH, Donaldson J, Chhanabhai M, Fitzgerald C, Gill K, Klasa R, MacPherson N, O’Reilly S, Spinelli JJ, Sutherland J, Wilson KS, Gascoyne RD, Connors JM (2005) Introduction of combined CHOP plus rituximab therapy dramatically improved outcome of diffuse large B-cell lymphoma in British Columbia. J Clin Oncol 23(22):5027–5033. doi:10.1200/JCO.2005.09.137
4. Pfreundschuh M, Trumper L, Osterborg A, Pettengell R, Trneny M, Imrie K, Ma D, Gill D, Walewski J, Zinzani PL, Stahel R, Kvaloy S, Shpilberg O, Jaeger U, Hansen M, Lehtinen T, Lopez-Guillermo A, Corrado C, Scheliga A, Milpied N, Mendila M, Rashford M, Kuhnt E, Loeffler M, MabThera International Trial G (2006) CHOP-like chemotherapy plus rituximab versus CHOP-like chemotherapy alone in young patients with good-prognosis diffuse large-B-cell lymphoma: a randomised controlled trial by the MabThera International Trial (MInT) Group. Lancet Oncol 7(5):379–391. doi:10.1016/S1470-2045(06)70664-7
5. The International Non-Hodgkin’s Lymphoma Prognostic Factors Project (1993) A predictive model for aggressive non-Hodgkin’s lymphoma. N Engl J Med 329(14):987–994. doi:10.1056/NEJM199309303291402
6. Hara T, Tsurumi H, Takemura M, Goto H, Yamada T, Sawada M, Takahashi T, Moriwaki H (2000) Serum-soluble fas level determines clinical symptoms and outcome of patients with aggressive non-Hodgkin’s lymphoma. Am J Hematol 64(4):257–261
7. Goto N, Tsurumi H, Takemura M, Hara T, Sawada M, Kasahara S, Kanemura N, Yamada T, Shimizu M, Takahashi T, Tomita E, Seishima M, Takami T, Moriwaki H (2006) Serum-soluble tumor necrosis factor receptor 2 (sTNF-R2) level determines clinical outcome in patients with aggressive non-Hodgkin’s lymphoma. Eur J Haematol 77(3):217–225. doi:10.1111/j.1600-0609.2006.00702.x
8. Goto H, Tsurumi H, Takemura M, Ino-Shimomura Y, Kasahara S, Sawada M, Yamada T, Hara T, Fukuno K, Goto N, Okuno M, Takami T, Seishima M, Moriwaki H (2005) Serum-soluble interleukin-2 receptor (sIL-2R) level determines clinical outcome in patients with aggressive non-Hodgkin’s lymphoma: in combination with the International Prognostic Index. J Cancer Res Clin Oncol 131(2):73–79. doi:10.1007/s00432-004-0600-9
9. Prado CM, Baracos VE, McCargar LJ, Mourtzakis M, Mulder KE, Reiman T, Butts CA, Scarfe AG, Sawyer MB (2007) Body composition as an independent determinant of 5-fluorouracil-based chemotherapy toxicity. Clin Cancer Res 13(11):3264–3268. doi:10.1158/1078-0432.CCR-06-3067
10. Prado CM, Lieffers JR, McCargar LJ, Reiman T, Sawyer MB, Martin L, Baracos VE (2008) Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol 9(7):629–635. doi:10.1016/S1470-2045(08)70153-0
11. Prado CM, Baracos VE, McCargar LJ, Reiman T, Mourtzakis M, Tonkin K, Mackey JR, Koski S, Pituskin E, Sawyer MB (2009) Sarcopenia as a determinant of chemotherapy toxicity and time to tumor progression in metastatic breast cancer patients receiving capecitabine treatment. Clin Cancer Res 15(8):2920–2926. doi:10.1158/1078-0432.CCR-08-2242
12. Tan BH, Birdsell LA, Martin L, Baracos VE, Fearon KC (2009) Sarcopenia in an overweight or obese patient is an adverse prognostic factor in pancreatic cancer. Clin Cancer Res 15(22):6973–6979. doi:10.1158/1078-0432.CCR-09-1525
13. Antoun S, Baracos VE, Birdsell L, Escudier B, Sawyer MB (2010) Low body mass index and sarcopenia associated with dose-limiting toxicity of sorafenib in patients with renal cell carcinoma. Ann Oncol 21(8):1594–1598. doi:10.1093/annonc/mdp605
14. Lanic H, Kraut-Tauzia J, Modzelewski R, Clatot F, Mareschal S, Picquenot JM, Stamatoullas A, Lepretre S, Tilly H, Jardin F (2014) Sarcopenia is an independent prognostic factor in elderly patients with diffuse large B-cell lymphoma treated with immunochemotherapy. Leuk Lymphoma 55(4):817–823. doi:10.3109/10428194.2013.816421
15. Tsurumi H, Yamada T, Sawada M, Kasahara S, Kanemura N, Kojima Y, Fukuno K, Hara T, Saio M, Takahashi T, Oyama M, Ozawa K, Takami T, Moriwaki H (2004) Biweekly CHOP or THP-COP regimens in the treatment of newly diagnosed aggressive non-Hodgkin’s lymphoma. A comparison of doxorubicin and pirarubicin: a randomized phase II study. J Cancer Res Clin Oncol 130(2):107–113. doi:10.1007/s00432-003-0508-9
16. Hara T, Tsurumi H, Goto N, Kitagawa J, Kanemura N, Yoshikawa T, Kasahara S, Goto H, Fukuno K, Yamada T, Sawada M, Yasuda I, Katsumura N, Takahashi T, Takami T, Moriwaki H (2010) Phase II study of rituximab combined with THP-COP as first-line therapy for patients younger than 70 years with diffuse large B cell lymphoma. J Cancer Res Clin Oncol 136(1):65–70. doi:10.1007/s00432-009-0637-x
17. Kasahara S, Hara T, Tsurumi H, Goto N, Kitagawa J, Kanemura N, Yoshikawa T, Goto H, Fukuno K, Yamada T, Sawada M, Takahashi T, Takami T, Moriwaki H (2011) Phase II study of the tetrahydropyranyl adriamycin-cyclophosphamide, vincristine, and prednisolone regimen combined with rituximab as first-line treatment for elderly patients with diffuse large B-cell lymphoma. Leuk Lymphoma 52(4):629–634. doi:10.3109/10428194.2011.555024
18. Carbone PP, Kaplan HS, Musshoff K, Smithers DW, Tubiana M (1971) Report of the committee on Hodgkin’s disease staging classification. Cancer Res 31(11):1860–1861
19. Sehn LH, Berry B, Chhanabhai M, Fitzgerald C, Gill K, Hoskins P, Klasa R, Savage KJ, Shenkier T, Sutherland J, Gascoyne RD, Connors JM (2007) The revised International Prognostic Index (R-IPI) is a better predictor of outcome than the standard IPI for patients with diffuse large B-cell lymphoma treated with R-CHOP. Blood 109(5):1857–1861. doi:10.1182/blood-2006-08-038257
20. Miller AA, Salewski E (1994) Prospects for pirarubicin. Med Pediatr Oncol 22(4):261–268
21. Takagi T, Oguro M (1987) (2″-R)-4′-o-Tetrahydropyranyladriamycin, a new anthracycline derivative: its effectiveness in lymphoid malignancies. Cancer Chemother Pharmacol 20(2):151–154
22. Tsurumi H, Hara T, Goto N, Kanemura N, Kasahara S, Sawada M, Yasuda I, Yamada T, Shimizu M, Takami T, Moriwaki H (2007) A phase II study of a THP-COP regimen for the treatment of elderly patients aged 70 years or older with diffuse large B-cell lymphoma. Hematol Oncol 25(3):107–114. doi:10.1002/hon.815
23. Sawada M, Tsurumi H, Yamada T, Hara T, Fukuno K, Goto H, Shimizu M, Kasahara S, Yoshikawa T, Kanemura N, Oyama M, Takami T, Moriwaki H (2002) A prospective study of P-IMVP-16/CBDCA: a novel salvage chemotherapy for patients with aggressive non-Hodgkin’s lymphoma who had previously received CHOP therapy as first-line chemotherapy. Eur J Haematol 68(6):354–361
24. Hirakawa T, Yamaguchi H, Yokose N, Gomi S, Inokuchi K, Dan K (2010) Importance of maintaining the relative dose intensity of CHOP-like regimens combined with rituximab in patients with diffuse large B-cell lymphoma. Ann Hematol 89(9):897–904. doi:10.1007/s00277-010-0956-7
25. Morley JE, Baumgartner RN, Roubenoff R, Mayer J, Nair KS (2001) Sarcopenia. J Lab Clin Med 137(4):231–243. doi:10.1067/mlc.2001.113504
26. Prado CM, Birdsell LA, Baracos VE (2009) The emerging role of computerized tomography in assessing cancer cachexia. Curr Opin Support Palliat Care 3(4):269–275. doi:10.1097/SPC.0b013e328331124a
27. Shen W, Punyanitya M, Wang Z, Gallagher D, St-Onge MP, Albu J, Heymsfield SB, Heshka S (2004) Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image. J Appl Physiol 97(6):2333–2338. doi:10.1152/japplphysiol.00744.2004
28. Mitsiopoulos N, Baumgartner RN, Heymsfield SB, Lyons W, Gallagher D, Ross R (1998) Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography. J Appl Physiol 85(1):115–122
29. Mourtzakis M, Prado CM, Lieffers JR, Reiman T, McCargar LJ, Baracos VE (2008) A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Appl Physiol Nutr Metab 33(5):997–1006. doi:10.1139/H08-075
30. Zweig MH, Campbell G (1993) Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine. Clin Chem 39(4):561–577
31. Kanda Y (2013) Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 48(3):452–458. doi:10.1038/bmt.2012.244
32. Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, Jatoi A, Loprinzi C, MacDonald N, Mantovani G, Davis M, Muscaritoli M, Ottery F, Radbruch L, Ravasco P, Walsh D, Wilcock A, Kaasa S, Baracos VE (2011) Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 12(5):489–495. doi:10.1016/S1470-2045(10)70218-7
33. Fearon KC, Glass DJ, Guttridge DC (2012) Cancer cachexia: mediators, signaling, and metabolic pathways. Cell Metab 16(2):153–166. doi:10.1016/j.cmet.2012.06.011
34. Richards CH, Roxburgh CS, MacMillan MT, Isswiasi S, Robertson EG, Guthrie GK, Horgan PG, McMillan DC (2012) The relationships between body composition and the systemic inflammatory response in patients with primary operable colorectal cancer. PLoS One 7(8):e41883. doi:10.1371/journal.pone.0041883
35. Argiles JM, Busquets S, Lopez-Soriano FJ (2005) The pivotal role of cytokines in muscle wasting during cancer. Int J Biochem Cell Biol 37(10):2036–2046. doi:10.1016/j.biocel.2005.03.014
36. Gabay C, Kushner I (1999) Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 340(6):448–454. doi:10.1056/NEJM199902113400607
37. Richards CH, Leitch EF, Horgan PG, Anderson JH, McKee RF, McMillan DC (2010) The relationship between patient physiology, the systemic inflammatory response and survival in patients undergoing curative resection of colorectal cancer. Br J Cancer 103(9):1356–1361. doi:10.1038/sj.bjc.6605919
38. Roxburgh CS, Platt JJ, Leitch EF, Kinsella J, Horgan PG, McMillan DC (2011) Relationship between preoperative comorbidity, systemic inflammatory response, and survival in patients undergoing curative resection for colorectal cancer. Ann Surg Oncol 18(4):997–1005. doi:10.1245/s10434-010-1410-8
39. McMillan DC, Canna K, McArdle CS (2003) Systemic inflammatory response predicts survival following curative resection of colorectal cancer. Br J Surg 90(2):215–219. doi:10.1002/bjs.4038
40. Aleman MR, Santolaria F, Batista N, de La Vega M, Gonzalez-Reimers E, Milena A, Llanos M, Gomez-Sirvent JL (2002) Leptin role in advanced lung cancer. A mediator of the acute phase response or a marker of the status of nutrition? Cytokine 19(1):21–26
41. Hanahan D, Coussens LM (2012) Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21(3):309–322. doi:10.1016/j.ccr.2012.02.022
42. Mamlouk S, Wielockx B (2013) Hypoxia-inducible factors as key regulators of tumor inflammation. Int J Cancer 132(12):2721–2729. doi:10.1002/ijc.27901
43. Dodson S, Baracos VE, Jatoi A, Evans WJ, Cella D, Dalton JT, Steiner MS (2011) Muscle wasting in cancer cachexia: clinical implications, diagnosis, and emerging treatment strategies. Annu Rev Med 62:265–279. doi:10.1146/annurev-med-061509-131248
44. Riihijarvi S, Taskinen M, Jerkeman M, Leppa S (2011) Male gender is an adverse prognostic factor in B-cell lymphoma patients treated with immunochemotherapy. Eur J Haematol 86(2):124–128. doi:10.1111/j.1600-0609.2010.01541.x
45. Carella AM, de Souza CA, Luminari S, Marcheselli L, Chiappella A, di Rocco A, Cesaretti M, Rossi A, Rigacci L, Gaidano G, Merli F, Spina M, Stelitano C, Hohaus S, Barbui A, Puccini B, Miranda EC, Guida A, Federico M (2013) Prognostic role of gender in diffuse large B-cell lymphoma treated with rituximab containing regimens: a Fondazione Italiana Linfomi/Grupo de Estudos em Molestias Onco-Hematologicas retrospective study. Leuk Lymphoma 54(1):53–57. doi:10.3109/10428194.2012.691482
46. Micheli A, Ciampichini R, Oberaigner W, Ciccolallo L, de Vries E, Izarzugaza I, Zambon P, Gatta G, De Angelis R, Group EW (2009) The advantage of women in cancer survival: an analysis of EUROCARE-4 data. Eur J Cancer 45(6):1017–1027. doi:10.1016/j.ejca.2008.11.008
47. Muller C, Murawski N, Wiesen MH, Held G, Poeschel V, Zeynalova S, Wenger M, Nickenig C, Peter N, Lengfelder E, Metzner B, Rixecker T, Zwick C, Pfreundschuh M, Reiser M (2012) The role of sex and weight on rituximab clearance and serum elimination half-life in elderly patients with DLBCL. Blood 119(14):3276–3284. doi:10.1182/blood-2011-09-380949
48. Riggio O, Angeloni S, Ciuffa L, Nicolini G, Attili AF, Albanese C, Merli M (2003) Malnutrition is not related to alterations in energy balance in patients with stable liver cirrhosis. Clin Nutr 22(6):553–559
49. Peng S, Plank LD, McCall JL, Gillanders LK, McIlroy K, Gane EJ (2007) Body composition, muscle function, and energy expenditure in patients with liver cirrhosis: a comprehensive study. Am J Clin Nutr 85(5):1257–1266
50. Alberino F, Gatta A, Amodio P, Merkel C, Di Pascoli L, Boffo G, Caregaro L (2001) Nutrition and survival in patients with liver cirrhosis. Nutrition 17(6):445–450
51. Gusella M, Toso S, Ferrazzi E, Ferrari M, Padrini R (2002) Relationships between body composition parameters and fluorouracil pharmacokinetics. Br J Clin Pharmacol 54(2):131–139
52. Cosqueric G, Sebag A, Ducolombier C, Thomas C, Piette F, Weill-Engerer S (2006) Sarcopenia is predictive of nosocomial infection in care of the elderly. Br J Nutr 96(5):895–901
53. Spina M, Balzarotti M, Uziel L, Ferreri AJ, Fratino L, Magagnoli M, Talamini R, Giacalone A, Ravaioli E, Chimienti E, Berretta M, Lleshi A, Santoro A, Tirelli U (2012) Modulated chemotherapy according to modified comprehensive geriatric assessment in 100 consecutive elderly patients with diffuse large B-cell lymphoma. Oncologist 17(6):838–846. doi:10.1634/theoncologist.2011-0417
54. Marchesi F, Cenfra N, Altomare L, Dessanti ML, Mecarocci S, Cerchiara E, Rago A, D’Andrea M, Tomarchio V, Olimpieri OM, Tirindelli MC, Mengarelli A, Petti MC, Avvisati G, Cimino G (2013) A retrospective study on 73 elderly patients (>/=75years) with aggressive B-cell non Hodgkin lymphoma: clinical significance of treatment intensity and comprehensive geriatric assessment. J Geriatr Oncol 4(3):242–248. doi:10.1016/j.jgo.2013.04.003
55. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinkova E, Vandewoude M, Zamboni M, European Working Group on Sarcopenia in Older P (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 39(4):412–423. doi:10.1093/ageing/afq034