Journal of Pain and Symptom Management
Volume 39, Issue 5 , Pages 859-871 , May 2010

Cancer-Related Symptom Clusters, Eosinophils, and Survival in Hepatobiliary Cancer: An Exploratory Study

  • Jennifer L. Steel, PhD

      Affiliations

    • Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA
    • Corresponding Author InformationAddress correspondence to: Jennifer L. Steel, PhD, University of Pittsburgh School of Medicine; 3459 Fifth Avenue; Pittsburgh, PA 15213, USA.
    • ,
  • Kevin H. Kim, PhD

      Affiliations

    • Department of Psychology in Education, University of Pittsburgh, Pittsburgh, Pennsylvania, USA
    • ,
  • Mary Amanda Dew, PhD

      Affiliations

    • Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA
    • ,
  • Mark L. Unruh, MD

      Affiliations

    • Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA
    • ,
  • Michael H. Antoni, PhD

      Affiliations

    • Department of Psychology, University of Miami, Miami, Florida, USA
    • ,
  • Marion C. Olek, MS, MPH

      Affiliations

    • University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA
    • ,
  • David A. Geller, MD

      Affiliations

    • Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA
    • ,
  • Brian I. Carr, MD, PhD, FRCP

      Affiliations

    • Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA
    • ,
  • Lisa H. Butterfield, PhD

      Affiliations

    • Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA
    • Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA
    • Department of Immunology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA
    • ,
  • T. Clark Gamblin, MD

      Affiliations

    • Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA

,Accepted 16 October 2009.

References 

  1. NIH Consensus Development Program . Symptom management in cancer: pain, depression, and fatigue. NIH Consensus State-of-Science Conference. July 6–17, 2002;
  2. Dodd M, Janson S, Facione N, et al. Advancing the science of symptom management. J Adv Nurs. 2001;33:668–676
  3. Barsevick AM, Whitmer K, Nail LM, Beck SL, Dudley WN. Symptom cluster research: conceptual, design, measurement, and analysis issues. J Pain Symptom Manage. 2006;31:85–95
  4. Miaskowski C, Dodd M, Lee K. Symptom clusters: the new frontier in symptom management research. J Natl Cancer Inst Monogr. 2004;32:17–21
  5. Dantzer R. Cytokine-induced sickness behavior: where do we stand?. Brain Behav Immun. 2001;15:7–24
  6. Cleeland CS, Bennett GJ, Dantzer R, et al. Are the symptoms of cancer and cancer treatment due to a shared biologic mechanism? A cytokine-immunologic model of cancer symptoms. Cancer. 2003;97:2919–2925
  7. Wiesseler-Frank J, Maier SF, Watkins LR. Central proinflammatory cytokines and pain enhancement. Neurosignals. 2005;14:166–174
  8. Sommer C, Kress M. Recent findings on how proinflammatory cytokines cause pain: peripheral mechanisms in inflammatory and neuropathic hyperalgesisa. Neurosci Lett. 2004;361:184–187
  9. McMahon SB, Cafferty WB, Marchand F. Immune and glial cell factors as pain mediators and modulators. Exp Neurol. 2005;192:444–462
  10. Logan HL, Lutgendorf S, Kirchner HL, Rivera EM, Lubaroff D. Pain and immunological response to root canal treatment and subsequent health outcomes. Psychosom Med. 2001;63:453–462
  11. Hori T, Oka T, Hosoi M, Aou S. Pain modulatory actions of cytokines and prostaglandin E2 in the brain. Ann N Y Acad Sci. 1998;840:269–281
  12. Kurzrock R. The role of cytokines in cancer-related fatigue. Cancer. 2001;92(6 Suppl):1684–1688
  13. Bower JE, Ganz PA, Aziz N, Fahey JL. Fatigue and proinflammatory cytokine activity in breast cancer survivors. Psychosom Med. 2002;64:604–611
  14. Dimeo F, Schmittel A, Fietz T, et al. Physical performance, depression, immune status and fatigue in patients with hematological malignancies after treatment. Ann Oncol. 2004;15:1237–1242
  15. Anisman AV, Ravindran J, Griffiths J, Merali Z. Endocrine and cytokine correlates of major depression and dysthymia with typical or atypical features. Mol Psychiatry. 1999;4:182–188
  16. Maes M. Major depression and activation of the inflammatory response system. Adv Exp Med Biol. 1999;461:25–46
  17. Musselman DL, Miller AH, Porter MR, et al. Higher than normal plasma interleukin-6 concentrations in cancer patients with depression: preliminary findings. Am J Psychiatry. 2001;158:1252–1257
  18. Sluzewska A. Indicators of immune activation in depressed patients. Adv Exp Med Biol. 1999;461:59–74
  19. Raison CL, Miller AH. Depression in cancer: new developments regarding diagnosis and treatment. Biol Psychiatry. 2003;54:283–294
  20. Besedovsky H, del Rey A, Sorkin E, Dinarello CA. Immunoregulatory feedback between interleukin-1 and glucocorticoid hormones. Science. 1986;233:652–654
  21. Rivier C. Influence of immune signals on the hypothalamic-pituitary axis of the rodent. Front Neuroendocrinol. 1995;16:151–182
  22. Pariante CM, Miller AH. Glucocorticoid receptions in major depression: relevance to pathophysiology and treatment. Biol Psychiatry. 2001;49:391–404
  23. Capuron JF, Gumnick DL, Musselman DH, et al. Neurobehavioral effects of interferon-alpha in cancer patients phenomenology and paroxetine responsiveness of symptoms dimensions. Neuropsychopharmacology. 2002;26:643–652
  24. Lestage J, Verrier D, Palin K, Dantzer R. The enzyme indoleamine 2,3-dioxygenase is induced in the mouse brain in response to peripheral administration of lipopolysaccharide and superantigen. Brain Behav Immun. 2002;16:596–601
  25. Liebau C, Baltzer AW, Schmidt S, et al. Interleukin-12 and interleukin-18 induce indoleamine 2,3-dioxygenase (IDO) activity in human osteosarcoma cell lines independently from interferon-gamma. Anticancer Res. 2002;22:931–936
  26. Suarez EC, Krishnan RR, Lewis JG. The relation of severity of depressive symptoms to monocyte-associated proinflammatory cytokines and chemokines in apparently healthy men. Psychosom Med. 2003;65:362–368
  27. Bonaccorso S, Puzella A, Marino V, Pasquini M. Immunotherapy with interferon-alpha in patients affected by chronic hepatitis C induces an intercorrelated stimulation of the cytokine network and an increase in depressive and anxiety symptoms. Psychiatry Res. 2001;105:45–55
  28. Swallow CJ, Partridge EA, Macmillan JC, et al. α2HS-glycoprotein, an antagonist of transforming growth factor ß in vivo, inhibits intestinal tumor progression. Cancer Res. 2004;64:6402–6409
  29. Lotfi R, Lee J, Lotze M. Eosinophilic granulocytes and damage-associated molecular pattern molecules (DAMPs): role in the inflammatory response within tumors. J Immunother. 2007;30:16–28
  30. Schwartz R. The hypereosinophilic syndrome and the biology of cancer. N Engl J Med. 2003;348:1199–1200
  31. Woodgett J. Recent advances in the protein kinase B signaling pathway. Curr Opin Cell Biol. 2005;17:150–157
  32. Griffin J, Leung J, Bruner R, Caligiuri M, Briesewitz R. Discovery of a fusion kinase in EOL-1 cells and idiopathic hypereosinophilic syndrome. Proc Natl Acad Sci U S A. 2003;100:7830–7835
  33. Davies S, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J. 2000;351:95–105
  34. Pastrnak A, Jansa P. Local eosinophilia in stroma of tumors related to prognosis. Neoplasma. 1984;31:323–326
  35. Rivoltini L, Colombo MP, Parmiani G, et al. In vitro anti-tumor activity of eosinophils from cancer patients treated with subcutaneous administration of interleukin 2. Role of interleukin 5. Int J Cancer. 1993;54:8–15
  36. Silberstein D, Schoof D, Rodrick M, et al. Activation of eosinophils in cancer patients treated with IL-2 and IL-2-generated lymphokine-activated killer cells. J Immunol. 1989;142:2162–2167
  37. Arinaga S, Karimine C, Takamuku K, et al. Correlation of eosinophilia with clinical response in patients with advanced carcinoma treated with low-dose recombinant interleukin-2 and mitomycin C. Cancer Immunol Immunother. 1992;35:246–250
  38. Lowe D, Jorizzo J, Hutt MS. Tumour-associated eosinophilia: a review. J Clin Pathol. 1981;34:1343–1348
  39. Sanderson C. Interleukin-5, eosinophils, and disease. Blood. 1992;79:3101–3109
  40. Shirai M, Watanabe S, Nishioka M. Depressed lymphokine-activated killer activity and analyses of the precursor cells in peripheral blood of patient with hepatocellular carcinoma. Hepatogastroenterology. 1990;37:465–468
  41. Shirai M, Watanabe S, Nishioka M. Intramural injection of OK432 and lymphokine-activated killer activity in peripheral blood of patients with hepatocellular carcinoma. Eur J Cancer. 1990;26:965–969
  42. Shirai M, Watanabe S, Nishioka M. Defective immunological functions associated with abnormal lymphokine-activated killer activity in patients with hepatocellular carcinoma. J Gastroenterol Hepatol. 1990;5:542–548
  43. Wang Y, Chen H, Wu M, et al. Postoperative immunotherapy for patients with hepatocarcinoma using tumor-infiltrating lymphocytes. Chin Med J. 1997;110:114–117
  44. Haruta I, Yamauchi K, Aruga A, et al. Analytical study of the clinical response to two distinct adoptive immunotherapies for advanced hepatocellular carcinoma: comparison between LAK cell and CTL therapy. J Immunother Emphasis Tumor Immunol. 1996;19:218–223
  45. Taketomi A, Shimada M, Shirabe K, et al. Natural killer cell activity in patients with hepatocellular carcinoma. Cancer. 1998;83:58–63
  46. Actis GC, Ponzetto A, D'Urso N, et al. Chronic active hepatitis. Interferon-activated natural killer like cells against a hepatoma cell line transfected with the hepatitis B virus nucleic acid. Liver. 1991;11:106–113
  47. Kawarabayashi N, Seki S, Hatsuse K, et al. Decrease of CD56(+)T cells and natural killer cells in cirrhotic livers with hepatitis C may be involved in their susceptibility to hepatocellular carcinoma. Hepatology. 2000;32:962–969
  48. Nakajima T, Mizushima N, Kanai K. Relationship between natural killer activity and development of hepatocellular carcinoma in patient with cirrhosis of the liver. Jpn J Clin Oncol. 1988;17:327–332
  49. Okanoue T, Itoh Y, Minami M, et al. Interferon therapy lowers the rate of progression to hepatocellular carcinoma in chronic hepatitis C but not significantly in an advanced stage: a retrospective study in 1148 patients. J Hepatol. 1999;30:653–659
  50. Fang Y, Wang L, Jin J, Zha X. Focal adhesion kinase affect the sensitivity of human hepatocellular carcinoma cell line SMMC-7721 to tumor necrosis factor-alpha/cycloheximide-induced apoptosis by regulating protein kinase B levels. Eur J Biochem. 2001;268:4513–4519
  51. Tsujimoto T, Kuriyama S, Yamazaki M, et al. Augmented hepatocellular carcinoma progression and depressed Kupffer cell activity in rat cirrhotic livers. Int J Oncol. 2001;18:41–47
  52. Wang D, Yang E, Cheng LY. Effects of IFN-gamma, TNF-alpha and EGF on expression of HLA class I antigen and the proliferation of human hepatocellular carcinoma HepG2 cells. Anticancer Res. 1997;17:181–188
  53. Feng X, Tang X, Zheng Z. Preliminary studies on the effects of tumor necrosis factor gene transfer on the growth of human hepatocellular carcinoma cells in nude mice. Chin J Oncol. 1995;17:167–169
  54. Osawa Y, Nagaki M, Banno Y, et al. Possible involvement of reactive oxygen species in D-galactosamine-induced sensitization against tumor necrosis factor-alpha induced hepatocyte apoptosis. J Cell Physiol. 2001;187:374–385
  55. Atarashi Y, Yasumura S, Nambu S, et al. A novel human tumor necrosis factor alpha mutein, F4614, inhibits in vitro and in vivo growth of murine and human hepatoma: implications for immunotherapy of hepatocellular carcinoma. Hepatology. 1998;28:57–67
  56. Cella DF, Tulsky DS, Gray G, et al. The Functional Assessment of Cancer Therapy scale: development and validation of the general measure. J Clin Oncol. 1993;11:570–579
  57. Heffernan N, Cella D, Webster K, et al. Measuring health-related quality of life in patients with hepatobiliary cancers: the functional assessment of cancer therapy-hepatobiliary questionnaire. J Clin Oncol. 2002;20:2229–2239
  58. Cleeland CS, Nakamura Y, Mendoza TR, et al. Dimensions of the impact of cancer pain in a four country sample: new information from multidimensional scaling. Pain. 1996;67:267–273
  59. Cella D. The Functional Assessment of Cancer Therapy-Anemia (FACT-An) scale: a new tool for the assessment of outcomes in cancer anemia and fatigue. Semin Hematol. 1997;34(Suppl 2):13–19
  60. Radloff LS. The Center for Epidemiological Studies depression scale: a self-report depression scale for research in the general population. Appl Psychol Meas. 1977;1:385–401
  61. Zhang T, Ramakrishnon R, Livny M. BIRCH: an efficient data clustering method for very large databases. Proceedings of the ACM SIGMOD Conference on Management of Data. Montreal, Canada: ACM; 1996;
  62. Chiu T, Fang D, Chen J, Wang Y, Jeris C. A robust and scalable clustering algorithm for mixed type attributes in large database environment. Proceedings of the Seventh ACM SIGKDD International Conference on Knowledge Discovery and Data Mining. San Francisco, CA: ACM.
  63. Jamshidian M, Bentler PM. ML estimation of mean and covariance structures with missing data using complete data routines. J Educ Behav Stat. 1999;24:21–41
  64. Yuan KH, Bentler PM. Three likelihood-based methods for mean and covariance structure analysis with nonnormal missing data. Sociol Methodol. 2000;30:165–200
  65. Hu L-T, Bentler PM. Fit indices in covariance structure modeling: sensitivity to underparameterized model misspecification. Psychol Methods. 1998;3:424–453
  66. Hu L-T, Bentler PM. Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Struct Equ Modeling. 1999;6:1–55
  67. Bentler PM. Comparative fit indexes in structural models. Psychol Bull. 1990;107:238–246
  68. Steiger JH, Lind JC. Statistically based tests for the number of common factors. Paper presented at the Psychometric Society, Iowa City, IA, 1980.
  69. Ahmad M, Rees R, Ali S. Escape from immunotherapy: possible mechanisms that influence tumor regression/progression. Cancer Immunol Immunother. 2004;53:844–854
  70. Noirot C, Leynadier F, Luce H, Abuaf N, Bernard PF. Hypereosinophilia in cancer and cirrhosis: utility of total eosinophil count, [French] Sem Hop. 1982;58:133–137
  71. Lucey D, Clerici M, Shearer G. Type 1 and type 2 cytokine dysregulation in human infectious, neoplastic, and inflammatory diseases. Clin Microbiol Rev. 1996;9:532–562

 This study was funded by grants from the American Cancer Society, the Pittsburgh Mind Body Center (National Institutes of Health grants HL065111, HL065112, HL076852, and HL076858), and the National Cancer Institute (5K07CA118576).

PII: S0885-3924(10)00142-9

doi: 10.1016/j.jpainsymman.2009.09.019

Journal of Pain and Symptom Management
Volume 39, Issue 5 , Pages 859-871 , May 2010

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