Skip to main content

Advertisement

SpringerLink
Log in

Correlation Between Immunoinflammatory Measures and Periostin Expression in Esophageal Squamous Cell Carcinoma: A Single-Center, Retrospective Cohort Study

  • Translational Research and Biomarkers
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Immunoinflammatory measures such as the neutrophil–lymphocyte ratio (NLR), the platelet–lymphocyte ratio (PLR), and the C-reactive protein (CRP)–albumin ratio (CAR) are useful prognostic measures in various malignancies. However, no study has investigated the correlation of these measures with microenvironmental inflammation. Periostin (POSTN), a small extracellular matrix protein, strongly associates with cancer microenvironmental inflammation. The current study investigated the correlation of NLR, PLR, and CAR with periostin expression in esophageal squamous cell carcinoma (ESCC).

Methods

The study retrospectively evaluated preoperative NLR, PLR, and CAR hematologically and POSTN immunohistochemically in 171 patients. The correlation of immunoinflammatory measures, POSTN expression, and survival outcomes was measured.

Results

The study showed a significant correlation of POSTN-positive expression with poor overall survival (OS) (P < 0.0001) and recurrence-free survival (RFS) (P = 0.03). The POSTN-positive group had higher PLR (189.6 ± 8 vs. 159.3 ± 12; P = 0.04) and CAR (0.36 ± 0.06 vs. 0.14 ± 0.09; P < 0.05) than the POSTN-negative group, whereas NLR did not differ between the two groups (3.27 ± 0.19 vs. 2.65 ± 0.28; P = 0.07). The uni- and multivariate analyses showed that POSTN-positive expression (hazard ratio [HR], 1.595; 95% confidence interval [CI], 0.770–3.031; P = 0.03), CAR (HR, 1.663; 95% CI, 1.016–2.764; P = 0.03), gender (HR, 2.303; 95% CI, 1.067–6.019; P = 0.03), and tumor depth (HR, 1.957; 95% CI, 1.122–3.526; P = 0.01) were independent prognostic factors.

Conclusions

Because POSTN-positive expression strongly correlates with immunoinflammatory measures, especially PLR and CAR, it is an independent prognostic factor in ESCC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.

    Article  Google Scholar 

  2. Gupta B, Kumar N. Worldwide incidence, mortality and time trends for cancer of the oesophagus. Eur J Cancer Prevent. 2017;26:107–118.

    Article  Google Scholar 

  3. Walsh S, Cook E, Goulder F, Justin T, Keeling N. Neutrophil–lymphocyte ratio as a prognostic factor in colorectal cancer. J Surg Oncol. 2005;91:181–4.

    Article  CAS  Google Scholar 

  4. Ishibashi Y, Tsujimoto H, Hiraki S, et al. Prognostic value of preoperative systemic immunoinflammatory measures in patients with esophageal cancer. Ann Surg Oncol. 2018;25:3288–99.

    Article  Google Scholar 

  5. Kudo A. Introductory review: periostin–gene and protein structure. Cell Mol life Sci. 2017;74:4259–68.

    Article  CAS  Google Scholar 

  6. Ohno F, Nakahara T, Kido-Nakahara M, et al. Periostin links skin inflammation to melanoma progression in humans and mice. Int J Mol Sci. 2019;20:169.

    Article  Google Scholar 

  7. Deng X, Ao S, Hou J, Li Z, Lei Y, Lyu G. Prognostic significance of periostin in colorectal cancer. Chin J Cancer Res. 2019;31:547.

    Article  Google Scholar 

  8. Brierley JD, Gospodarowicz MK, Wittekind C TNM Classification of Malignant Tumours. Oxford: Wiley; 2017

    Google Scholar 

  9. Ando N, Kato H, Igaki H, et al. A randomized trial comparing postoperative adjuvant chemotherapy with cisplatin and 5-fluorouracil versus preoperative chemotherapy for localized advanced squamous cell carcinoma of the thoracic esophagus (JCOG9907). Ann Surg Oncol. 2012;19:68–74.

    Article  Google Scholar 

  10. Schisterman EF, Perkins NJ, Liu A, Bondell H. Optimal cut-point and its corresponding Youden Index to discriminate individuals using pooled blood samples. Epidemiology. 2005;16:73–81.

    Article  Google Scholar 

  11. Shinto E, Tsuda H, Ueno H, et al. Prognostic implication of laminin-5 gamma 2 chain expression in the invasive front of colorectal cancers, disclosed by area-specific four-point tissue microarrays. Lab Invest. 2005;85:257.

    Article  CAS  Google Scholar 

  12. Ishibashi Y, Tsujimoto H, Yaguchi Y, Kishi Y, Ueno H. Prognostic significance of systemic inflammatory markers in esophageal cancer: systematic review and meta-analysis. Ann Gastroenterol Surg. 2019;4:56–63.

    Article  Google Scholar 

  13. Chen M-F, Chen P-T, Kuan F-C, Chen W-C. The predictive value of pretreatment neutrophil-to-lymphocyte ratio in esophageal squamous cell carcinoma. Ann Surg Oncol. 2019;26:190–9.

    Article  Google Scholar 

  14. Horiuchi K, Amizuka N, Takeshita S, et al. Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor β. J Bone Miner Res. 1999;14:1239–49.

    Article  CAS  Google Scholar 

  15. Underwood TJ, Hayden AL, Derouet M, et al. Cancer-associated fibroblasts predict poor outcome and promote periostin-dependent invasion in oesophageal adenocarcinoma. J Pathol. 2015;235:466–77.

    Article  CAS  Google Scholar 

  16. Ma H, Wang J, Zhao X, et al. Periostin promotes colorectal tumorigenesis through integrin-FAK-Src pathway-mediated YAP/TAZ activation. Cell Rep. 2020;30:793–806.e796.

    Google Scholar 

  17. Moniuszko T, Wincewicz A, Koda M, Domysławska I, Sulkowski S. Role of periostin in esophageal, gastric, and colon cancer. Oncol Lett. 2016;12:783–7.

    Article  CAS  Google Scholar 

  18. Koh S-J, Choi Y, Kim BG, et al. Matricellular protein periostin mediates intestinal inflammation through the activation of nuclear factor κB signaling. PloS One. 2016;11:e0149652

    Article  Google Scholar 

  19. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420:860–7.

    Article  CAS  Google Scholar 

  20. Wang W, Sun Q-K, He Y-F, et al. Overexpression of periostin is significantly correlated to the tumor angiogenesis and poor prognosis in patients with esophageal squamous cell carcinoma. Int J Clin Exp Pathol. 2014;7:593.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Jia W, Wang W, Ji C-S, et al. Coexpression of periostin and EGFR in patients with esophageal squamous cell carcinoma and their prognostic significance. Onco Targets Ther. 2016;9:5133.

    Article  CAS  Google Scholar 

  22. Huang C, Yang G, Jiang T, Huang K, Cao J, Qiu Z. Effects of IL-6 and AG490 on regulation of Stat3-signaling pathway and invasion of human pancreatic cancer cells in vitro. J Exp Clin Cancer Res. 2010;29:51.

    Article  CAS  Google Scholar 

  23. Tu B, Du L, Fan Q-M, Tang Z, Tang T-T. STAT3 activation by IL-6 from mesenchymal stem cells promotes the proliferation and metastasis of osteosarcoma. Cancer Lett. 2012;325:80–8.

    Article  CAS  Google Scholar 

  24. Walter M, Liang S, Ghosh S, Hornsby PJ, Li R. Interleukin 6 secreted from adipose stromal cells promotes migration and invasion of breast cancer cells. Oncogene. 2009;28:2745–55.

    Article  CAS  Google Scholar 

  25. Tsujimoto H, Ono S, Ichikura T, Matsumoto Y, Yamamoto J, Hase K. Roles of inflammatory cytokines in the progression of gastric cancer: friends or foes? Gastric Cancer. 2010;13:212–21.

    Article  CAS  Google Scholar 

  26. Del Giudice M, Gangestad SW. Rethinking IL-6 and CRP: why they are more than inflammatory biomarkers, and why it matters. Brain Behav Immun. 2018;70:61–75.

    Article  Google Scholar 

  27. Chen Z, Sun H, Yue B, Li JH. Expressions and clinical significance of periostin, VEGF, ET-1, and Hs-CRP in patients with acute coronary syndrome. Jiangsu Med J. 2013;39:929–31.

    CAS  Google Scholar 

  28. Dixon MR, Haukoos JS, Udani SM, et al. Carcinoembryonic antigen and albumin predict survival in patients with advanced colon and rectal cancer. Arch Surg. 2003;138:962–6.

    Article  Google Scholar 

  29. Kaysen GA, Chertow GM, Adhikarla R, Young B, Ronco C, Levin NW. Inflammation and dietary protein intake exert competing effects on serum albumin and creatinine in hemodialysis patients. Kidney Int. 2001;60:333–40.

    Article  CAS  Google Scholar 

  30. Bologa RM, Levine DM, Parker TS, et al. Interleukin-6 predicts hypoalbuminemia, hypocholesterolemia, and mortality in hemodialysis patients. Am J Kidney Dis. 1998;32:107–14.

    Article  CAS  Google Scholar 

Download references

Funding

None.

Author information

Authors and Affiliations

  1. Department of Surgery, National Defense Medical College, Tokorozawa, Saitama, Japan

    Yusuke Ishibashi MD, Hironori Tsujimoto MD, PhD, Takahiro Einama MD, PhD, Satsuki Mochizuki PhD, Keita Kouzu MD, Shinsuke Nomura MD, Nozomi Ito MD, Manabu Harada MD, Hidekazu Sugasawa MD, PhD, Eiji Shinto MD, PhD, Yoji Kishi MD, PhD & Hideki Ueno MD, PhD

Authors
  1. Yusuke Ishibashi MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hironori Tsujimoto MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takahiro Einama MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Satsuki Mochizuki PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Keita Kouzu MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shinsuke Nomura MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nozomi Ito MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Manabu Harada MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hidekazu Sugasawa MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Eiji Shinto MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yoji Kishi MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Hideki Ueno MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hironori Tsujimoto MD, PhD.

Ethics declarations

Disclosure

There are no conflicts of interest.

Informed Consent

Written informed consent was obtained from all patients

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

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ishibashi, Y., Tsujimoto, H., Einama, T. et al. Correlation Between Immunoinflammatory Measures and Periostin Expression in Esophageal Squamous Cell Carcinoma: A Single-Center, Retrospective Cohort Study. Ann Surg Oncol 28, 1228–1237 (2021). https://doi.org/10.1245/s10434-020-08765-3

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-020-08765-3

Search

Navigation