Skip to main content

Advertisement

SpringerLink
Log in

The Influence of the Perioperative Nutritional Status on the Survival Outcomes for Esophageal Cancer Patients with Neoadjuvant Chemotherapy

  • Thoracic Oncology
  • Published:
Annals of Surgical Oncology Aims and scope Submit manuscript

Abstract

Background

Studies have shown a variety of nutritional indices to be prognostic predictors for esophageal cancer patients. However, which nutritional index should be used and when it should be measured during the perioperative period remain unclear. This study attempted to clarify the details surrounding predictive nutritional evaluation by assessing the longitudinal data of serologic indices in perioperative esophageal cancer patients.

Methods

The study included 141 esophageal cancer patients who underwent neoadjuvant chemotherapy after radical esophagectomy at Tohoku University Hospital from April 2008 to December 2017. The nutritional status was retrospectively assessed during the perioperative period, and the prognostic factors related to survival were analyzed.

Results

Use of the controlling nutritional status (CONUT) score showed that malnutrition occurred only from 14 days after surgery in most cases. Use of the prognostic nutritional index (PNI) showed that the ratio of malnutrition increased gradually from presurgery to 14 days after surgery. The timing of malnutrition that affected survival was 14 days after surgery with the CONUT score and presurgery and 4 months after surgery with the PNI. A multivariable analysis of independent prognostic factors predicting survival identified malnutrition 14 days after surgery with the CONUT score and a low PNI before surgery, invasion depth of the primary lesion, and node metastasis.

Conclusions

Malnutrition occurring during the perioperative state of esophageal cancer was shown to be a survival prognostic factor. Development of an optimal nutritional intervention is recommended for esophageal cancer patients to prevent malnutrition both before and after surgery.

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

Similar content being viewed by others

References

  1. Arends J, Baracos V, Bertz H, et al. ESPEN expert group recommendations for action against cancer-related malnutrition. Clin Nutr. 2017;36:1187–96.

    Article  CAS  Google Scholar 

  2. 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 

  3. Gebski V, Burmeister B, Smithers BM, Foo K, Zalcberg J, Simes J. Australasian Gastro-Intestinal Trials Group. Survival benefits from neoadjuvant chemoradiotherapy or chemotherapy in oesophageal carcinoma: a meta-analysis. Lancet Oncol. 2007;8:226–34.

    Article  CAS  Google Scholar 

  4. Nagaraja V, Cox MR, Eslick GD. Safety and efficacy of esophageal stents preceding or during neoadjuvant chemotherapy for esophageal cancer: a systematic review and meta-analysis. J Gastrointest Oncol. 2014;5:119–26.

    PubMed  PubMed Central  Google Scholar 

  5. Weimann A, Braga M, Carli F, et al. ESPEN guideline: clinical nutrition in surgery. Clin Nutr. 2017;36:623–50.

    Article  Google Scholar 

  6. Capra S, Ferguson M, Ried K. Cancer: impact of nutrition intervention outcome: nutrition issues for patients. Nutrition. 2001;17:769–72.

    Article  CAS  Google Scholar 

  7. Lanuti M, DeDelva P, Morse CR, et al. Management of delayed gastric emptying after esophagectomy with endoscopic balloon dilatation of the pylorus. Ann Thorac Surg. 2011;91:1019–24.

    Article  Google Scholar 

  8. Ignacio de Ulíbarri J, González-Madroño A, de Villar NG, et al. CONUT: a tool for controlling nutritional status: first validation in a hospital population. Nutr Hosp. 2005;20:38–45.

    PubMed  Google Scholar 

  9. Onodera T, Goseki N, Kosakim G. Prognostic nutritional index in gastrointestinal surgery of malnourished cancer patients. Nihon Geka Zasshi. 1984;85:1001–5.

    CAS  Google Scholar 

  10. Yoshida N, Baba Y, Shigaki H, et al. Preoperative nutritional assessment by controlling nutritional status (CONUT) is useful to estimate postoperative morbidity after esophagectomy for esophageal cancer. World J Surg. 2016;40:1910–7.

    Article  Google Scholar 

  11. Yoshida N, Harada K, Baba Y, et al. Preoperative controlling nutritional status (CONUT) is useful to estimate the prognosis after esophagectomy for esophageal cancer. Langenbecks Arch Surg. 2017;402:333–41.

    Article  Google Scholar 

  12. Nakatani M, Migita K, Matsumoto S, et al. Prognostic significance of the prognostic nutritional index in esophageal cancer patients undergoing neoadjuvant chemotherapy. Dis Esophagus. 2017;30:1–7.

    Article  CAS  Google Scholar 

  13. Matsumoto H, Okamoto Y, Kawai A, et al. Prognosis prediction for postoperative esophageal cancer patients using Onodera’s Prognostic Nutritional Index. Nutr Cancer. 2017;69:849–54.

    Article  Google Scholar 

  14. Okadome K, Baba Y, Yagi T, et al. Prognostic nutritional index, tumor-infiltrating lymphocytes, and prognosis in patients with esophageal cancer. Ann Surg. 2018. https://doi.org/10.1097/SLA.0000000000002985.

    Article  PubMed  Google Scholar 

  15. NCCN guidelines: esophageal and esophagogastric junction cancers. Retrieved 23 Jan 2019 at http://www.nccn.org/professionals/physician_gls/f_guidelines.asp#site.

  16. Brierley JD, Gospodarowicz MK, Wittekind C. TNM classification of malignant tumours. 8th ed. Wiley, Oxford; 2017.

    Google Scholar 

  17. Ichikawa H, Miyata G, Miyazaki S, et al. Esophagectomy using a thoracoscopic approach with an open laparotomic or hand-assisted laparoscopic abdominal stage for esophageal cancer: analysis of survival and prognostic factors in 315 patients. Ann Surg. 2013;257:873–85.

    Article  Google Scholar 

  18. Teshima J, Miyata G, Kamei T, et al. Comparison of short-term outcomes between prone and lateral decubitus positions for thoracoscopic esophagectomy. Surg Endosc. 2015;29:2756–62.

    Article  Google Scholar 

  19. Japan Esophageal Society. Japanese Classification of Esophageal Cancer, 11th edition: parts II and III. Esophagus. 2017;14:37–65.

    Article  Google Scholar 

  20. National Cancer Institute. Common Terminology Criteria for Adverse Events (CTCAE), version 4.0. U.S. Department of Health and Human Services, National Institutes of Health, Bethesda, MD, 2010. Retrieved 23 Jan 2019 at https://cabig-kc.nci.nih.gov/Vocab/KC/index.php/CTCAE.

  21. Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien–Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187–96.

    Article  Google Scholar 

  22. Chen P, Han L, Wang C, et al. Preoperative serum lipids as prognostic predictors in esophageal squamous cell carcinoma patients with esophagectomy. Oncotarget. 2017;8:41605–19.

    PubMed  PubMed Central  Google Scholar 

  23. Lee H, Jeong CW, Kwak C, et al. Preoperative cholesterol level is associated with worse pathological outcomes and postoperative survival in localized renal cell carcinoma patients: a propensity score-matched study. Clin Genitourin Cancer. 2017;15:e935–41.

    Article  Google Scholar 

  24. Lee SH, Lee JY, Hong TH, Kim BO, Lee YJ, Lee JG. Severe persistent hypocholesterolemia after emergency gastrointestinal surgery predicts in-hospital mortality in critically ill patients with diffuse peritonitis. PLoS ONE. 2018;13:e0200187.

    Article  Google Scholar 

  25. Baba Y, Yoshida N, Shigaki H, et al. Prognostic impact of postoperative complications in 502 patients with surgically resected esophageal squamous cell carcinoma: a retrospective single-institution study. Ann Surg. 2016;264:305–11.

    Article  Google Scholar 

  26. Goense L, Meziani J, Ruurda JP, van Hillegersberg R. Impact of postoperative complications on outcomes after oesophagectomy for cancer. Br J Surg. 2019;106:111–9.

    Article  CAS  Google Scholar 

  27. Kanekiyo S, Takeda S, Iida M, et al. Efficacy of perioperative immunonutrition in esophageal cancer patients undergoing esophagectomy. Nutrition. 2019;59:96–102.

    Article  Google Scholar 

  28. Wu N, Chen G, Hu H, Pang L, Chen Z. Low pretherapeutic serum albumin as a risk factor for poor outcome in esophageal squamous cell carcinomas. Nutr Cancer. 2015;67:481–5.

    Article  CAS  Google Scholar 

  29. Tan Z, Zhang M, Han Q, et al. A novel blood tool of cancer prognosis in esophageal squamous cell carcinoma: the fibrinogen/albumin ratio. J Cancer. 2017;8:1025–9.

    Article  CAS  Google Scholar 

  30. Yamana I, Takeno S, Shimaoka H, et al. Geriatric Nutritional Risk Index as a prognostic factor in patients with esophageal squamous cell carcinoma: retrospective cohort study. Int J Surg. 2018;56:44–8.

    Article  Google Scholar 

  31. Mitzman B, Schipper PH, Edwards MA, Kim S, Ferguson MK. Complications after esophagectomy are associated with extremes of body mass index. Ann Thorac Surg. 2018;106:973–80.

    Article  Google Scholar 

  32. Wightman SC, Posner MC, Patti MG, et al. Extremes of body mass index and postoperative complications after esophagectomy. Dis Esophagus. 2017;30:1–6.

    Article  CAS  Google Scholar 

  33. Ida S, Watanabe M, Karashima R, et al. Changes in body composition secondary to neoadjuvant chemotherapy for advanced esophageal cancer are related to the occurrence of postoperative complications after esophagectomy. Ann Surg Oncol. 2014;21:3675–9.

    Article  Google Scholar 

  34. Reisinger KW, Bosmans JW, Uittenbogaart M, et al. Loss of skeletal muscle mass during neoadjuvant chemoradiotherapy predicts postoperative mortality in esophageal cancer surgery. Ann Surg Oncol. 2015;22:4445–52.

    Article  Google Scholar 

  35. Ida S, Watanabe M, Yoshida N, et al. Sarcopenia is a predictor of postoperative respiratory complications in patients with esophageal cancer. Ann Surg Oncol. 2015;22:4432–7.

    Article  Google Scholar 

  36. Paireder M, Asari R, Kristo I, et al. Impact of sarcopenia on outcome in patients with esophageal resection following neoadjuvant chemotherapy for esophageal cancer. Eur J Surg Oncol. 2017;43:478–84.

    Article  CAS  Google Scholar 

  37. Miyata H, Yano M, Yasuda T, et al. Randomized study of clinical effect of enteral nutrition support during neoadjuvant chemotherapy on chemotherapy-related toxicity in patients with esophageal cancer. Clin Nutr. 2012;31:330–6.

    Article  Google Scholar 

  38. Taniguchi H, Sasaki T, Fujita H, et al. Effects of goal-directed fluid therapy on enhanced postoperative recovery: an interventional comparative observational study with a historical control group on oesophagectomy combined with ERAS program. Clin Nutr ESPEN. 2018;23:184–93.

    Article  Google Scholar 

Download references

Acknowledgment

This study did not receive any specific grant from any funding agencies in the public, commercial, or not-for-profit sectors. No preregistration was conducted for the study reported in this article.

Author information

Authors and Affiliations

  1. Department of Surgery, Tohoku University Hospital, Sendai, Japan

    Makoto Hikage MD, PhD, Yusuke Taniyama MD, PhD, Tadashi Sakurai MD, PhD, Chiaki Sato MD, PhD, Kai Takaya MD, PhD, Hiroshi Okamoto MD, PhD, Takuro Konno MD, PhD, Naoto Ujiie MD, PhD, Takeshi Naitoh MD, PhD, Michiaki Unno MD, PhD & Takashi Kamei MD, PhD

Authors
  1. Makoto Hikage MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yusuke Taniyama MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tadashi Sakurai MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chiaki Sato MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kai Takaya MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hiroshi Okamoto MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Takuro Konno MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Naoto Ujiie MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Takeshi Naitoh MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Michiaki Unno MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Takashi Kamei MD, PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Makoto Hikage MD, PhD.

Ethics declarations

Disclosure

There are no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 109 kb)

Supplementary Fig.

 1. Survival curves according to the nutrition score-based malnutrition groups derived using the Kaplan–Meier method. a The overall survival (OS) according to the prognostic nutritional index (PNI) pre-surgery (P = 0.066). b The OS according to the PNI four months after surgery (P = 0.069). (TIFF 15250 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hikage, M., Taniyama, Y., Sakurai, T. et al. The Influence of the Perioperative Nutritional Status on the Survival Outcomes for Esophageal Cancer Patients with Neoadjuvant Chemotherapy. Ann Surg Oncol 26, 4744–4753 (2019). https://doi.org/10.1245/s10434-019-07742-9

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1245/s10434-019-07742-9

Search

Navigation