Research ArticleClinical Studies

The Systemic Inflammation Score Is an Independent Prognostic Factor for Esophageal Cancer Patients who Receive Curative Treatment

TORU AOYAMA, MIHWA JU, KEISUKE KOMORI, HIROSHI TAMAGAWA, AYAKO TAMAGAWA, YUKIO MAEZAWA, ITARU HASHIMOTO, KAZUKI KANO, KENTARO HARA, HARUHIKO CHO, KENKI SEGAMI, DAISUKE MACHIDA, MASATO NAKAZONO, TAKASHI OSHIMA, NORIO YUKAWA and YASUSHI RINO
Anticancer Research May 2022, 42 (5) 2711-2717; DOI: https://doi.org/10.21873/anticanres.15749

Abstract

Background/Aim: Perioperative systemic inflammation affects the long-term oncological outcomes in cases of malignancies. We evaluated the clinical impact of the preoperative systemic inflammation score (SIS) in resectable esophageal cancer patients who received curative treatment. Patients and Methods: This study included 168 patients who underwent curative surgery followed by perioperative adjuvant chemotherapy for esophageal cancer between 2005 and 2018. The risk factors for overall survival (OS) and recurrence-free survival (RFS) were identified. Results: Based on the 3- and 5-year OS rate, we set the cut-off value for SIS at 2 in the preset study. Among the 168 total patients, 119 were categorized as the Low-SIS group, and 49 were categorized as the High-SIS group. The respective 3- and 5-year OS rates were 61.9% and 52.4% in the Low-SIS group and 33.3% and 26.6% in the High-SIS group. There were significant differences in OS (p<0.001). The SIS was therefore selected for the final multivariate analysis model (hazard ratio=2.094, 95% confidence interval=1.355-3.234, p<0.001). On comparing the perioperative clinical course between the High- and Low-SIS groups, there were significant differences in the rate of postoperative anastomosis leakage of grade ≥2 between the groups (61.5% in the High-SIS group vs. 30.3% in the Low-SIS group; p=0.021). Conclusion: The systemic inflammation score had a clinical effect on the long-term oncological outcomes in esophageal cancer patients, suggesting that it might be a promising prognostic factor for esophageal cancer patients.

Key Words:

Esophageal cancer is the eighth-most common cancer and the sixth leading cause of cancer-related mortality worldwide (1, 2). Perioperative adjuvant treatment and curative esophagectomy are the standard treatments for resectable esophageal cancer (3, 4). Although the long-term oncological outcomes of esophageal cancer patients have improved, half of resectable esophageal cancer patients experience recurrence despite curative treatment. To improve the long-term oncological outcomes of esophageal cancer patients, it is necessary to identify those patients likely to need more aggressive treatment.

Perioperative systemic inflammation is known to affect the long-term oncological outcomes in malignancies (5-8). Previous reports have shown that perioperative systemic inflammation affects the development of postoperative surgical complications and malnutrition (9, 10). In addition, postoperative surgical stress due to complications and malnutrition stimulate and enhance the growth of micrometastases and thus influence the long-term oncological outcomes. Therefore, if physicians were able to detect perioperative systemic inflammation before treatment, they could select minimally invasive surgery or perioperative nutritional treatment. However, tools for evaluating perioperative systemic inflammation for esophageal cancer patients are limited at present.

Recently, the systemic inflammation score (SIS) was developed and reported as a promising prognostic factor in gastric and pancreatic cancers (11, 12). The SIS consists of the serum albumin (Alb) level and lymphocyte-to-monocyte ratio (LMR) and thus has some clinical advantages over previous reported scores, such as ease of implementation, preoperative accessibility, and a low cost.

Given the above, we hypothesized that the preoperative SIS might have clinical influence on the clinical course and risk of recurrence in esophageal cancer patients who receive curative treatment. To confirm our hypothesis, we evaluated the prognostic value and clinical influence of the SIS in esophageal cancer patients who received curative treatment.

Patients and Methods

Patients. Patients were selected from the medical records of consecutive patients diagnosed with primary esophageal adenocarcinoma or squamous cell carcinoma and who underwent complete resection at Yokohama City University from 2005 to 2018.

Inclusion criteria were as follows: 1) stage I to III disease as evaluated according to the 7th edition of UICC classification, 2) complete (R0) resection of the esophageal cancer with lymphadenectomy, and 3) a laboratory blood analysis performed within one week before surgery. Patients who received R1 or R2 resection were excluded from the present analysis.

Surgical procedure. In principle, subtotal esophagectomy via right thoracotomy and reconstruction with a gastric tube is the standard procedure. Two-field lymph node dissection was indicated when tumors are located at the middle to lower thoracic esophagus, whereas three-field dissection was performed for upper thoracic tumors.

Measurement of the SIS. SIS was calculated by the perioperative Alb level and LMR. According to previous studies, a score of 0 was defined as Alb ≥4.0 g/dl and LMR ≥4.44, a score of 1 was defined as either Alb <4.0 g/dl or LMR <4.44, and a score of 2 was defined as Alb <4.0 g/dl and LMR <4.44. The SIS was assessed within seven days before surgery (13).

Evaluations and statistical analyses. The significance of differences between the SIS and clinicopathological parameters was determined using the χ2 test. The Kaplan–Meier method was used to generate the overall survival (OS) and recurrence-free survival (RFS) curves. OS was defined as the period between the date of surgery and death, and RFS was defined as the period between surgery and the occurrence of an event, recurrence, or death, whichever came first. The data of patients who had not experienced an event were censored at the date of the final observation. The univariate and multivariate survival analyses were performed using a Cox proportional hazards model. p-Values of <0.05 were considered to indicate statistical significance.

The SPSS software program (v26.0 J Win; SPSS, Chicago, IL, USA) was used for all of the statistical analyses. This study was approved by the IRB of Yokohama City University.

Results

Patients. A total of 168 patients were evaluated in the present study. Based on the 3- and 5-year OS rate, we set the cut-off value for the SIS at 2 in the preset study (Table I). Among 168 total patients, 119 (70.9%) were categorized as the Low-SIS group, and 49 (29.1%) were categorized as the High-SIS group.

View this table:
Table I.

Comparison of overall survival rates stratified by patient characteristics.

On comparing the patients’ background characteristics between the Low- and High-SIS groups, the findings were quite similar. Between the Low- and High-SIS groups, the median age (67.5 years old vs. 66.9 years old, p=0.669), incidence of males (84.0% vs. 87.8%, p=0.538), proportion with an alcohol habit (86.6% vs. 91.8%, p=0.337), proportion with a smoking habit (86.6% vs. 85.7%, p=0885), incidence of hypertension (46.2% vs. 51.0%, p=0.571), incidence of diabetes merits (16.8% vs. 11.1%, p=0.274), and incidence of chronic obstructive pulmonary disease (32.8% vs. 28.5%, p=0.594) were similar, while the median body mass index was significantly higher in the High-SIS group than in the Low-SIS group (21.5 vs. 20.5, p=0.046).

Survival analyses between the Low- and High-SIS groups. The respective 3- and 5-year OS rates were 61.9% and 52.4% in the Low-SIS group and 33.3% and 26.6% in the High-SIS group, showing a significant difference (Figure 1) (p<0.001). Each clinicopathological factor was categorized as shown in Table II and analyzed for its prognostic significance. The univariate analyses for the OS showed that the pathological T status and SIS were significant prognostic factors. The SIS was therefore selected for the final multivariate analysis model [hazard ratio (HR)=2.094, 95% confidence interval (CI)=1.355-3.234, p<0.001].

Figure 1.
Figure 1.

A comparison of the overall survival in the High-systemic inflammation score (SIS) and Low-SIS groups.

View this table:
Table II.

Uni- and multi-variate Cox proportional hazards analysis of clinicopathological factors for overall survival.

The respective 3- and 5-year RFS rates were 45.3% and 39.4%, respectively, in the Low-SIS group and 21.4% and 15.3%, respectively, in the High-SIS group, showing a significant difference (Figure 2) (p<0.001). Each clinicopathological factor was categorized as shown in Table III and analyzed for its prognostic significance. The univariate analyses for the RFS showed that the pathological T status and SIS were significant prognostic factors. The SIS was therefore also selected for the final multivariate analysis model (HR=1.983, 95%CI=1.328-2.962, p<0.001).

Figure 2.
Figure 2.

A comparison of the recurrence-free survival in the High-systemic inflammation score (SIS) and Low-SIS groups.

View this table:
Table III.

Uni- and multi-variate Cox proportional hazards analysis of clinicopathological factors for recurrence-free survival.

On comparing the recurrence site, there were significance differences in the rates of hematological recurrence and local recurrence between the High- and Low-SIS groups (Table IV).

View this table:
Table IV.

Patterns of recurrence according to systemic inflammation score.

A comparison of the postoperative clinical course between the Low- and High-SIS groups. On comparing the perioperative clinical course between the Low- and High-SIS groups, the perioperative clinical course was similar. The median values for the perioperative hospital stay (44 days vs. 47 days, p=0.771), operation time, and intraoperative blood loss (678 ml vs. 751 ml, p=0.520) were similar between the Low- and High-SIS groups. In addition, the incidence of postoperative surgical complications of grade ≥2 according to the Clavien-Dindo classification was also similar between the groups [Low- and High-SIS groups: 71.4% (35/49) vs. 72.2% (86/119), p=0.912]. In contrast, there were significant differences in the rate of postoperative anastomosis leakage of grade ≥2 according to the Clavien-Dindo classification [61.5% (23/39) in the High-SIS group vs. 30.3% (36/119) in the Low-SIS group; p=0.021].

Discussion

The present study clarified whether or not the SIS had clinical influence on the outcomes of esophageal cancer patients who received curative treatment. The major finding was that the preoperative SIS affects long-term oncological outcomes in esophageal cancer patients who receive curative treatment. Therefore, our results suggested that perioperative SIS is a promising prognostic factor for esophageal cancer patients.

In the present study, the 5-year OS rates were 52.4% in the Low-SIS group and 26.6% in the High-SIS group. Furthermore, the HR of the SIS for the OS was 2.094. Similar results have been observed in limited studies. Nomoto et al. evaluated the prognostic value of the adapted SIS (aSIS) in 509 esophageal squamous cell carcinoma patients (14), finding that the 3-year OS was 84.1% in the aSIS score 0 group, 74.6% in the aSIS score 1 group, and 57.3% in the aSIS score 2 group. In addition, they also showed that the 3-years cancer-specific survival (CSS) was 87.5% for aSIS 0, 81.3% for aSIS 1, and 72.0% for aSIS 2. The aSIS was shown to be a prognostic factor, and the HR of the aSIS for the OS was 1.81 (95%CI=1.16-2.81, p<0.01). Fu et al. investigated the clinical impact of the preoperative SIS in 357 esophageal squamous cell carcinoma patients (15). They demonstrated that the 5-years OS was 61% for SIS score 0, 50% for SIS score 1, and 35% for SIS score 2. The SIS was a prognostic factor, and the HR of the SIS for the OS was 1.24 (95%CI=1.05-1.43, p=0.029). Given these previous findings, the preoperative SIS appears to be a promising prognostic factor for esophageal cancer patients who receive curative treatment.

The impact of the preoperative SIS on the long-term oncological outcomes is possibly related to the occurrence of infectious complications, such as anastomosis leakage or pneumonia. In the present study, the rate of occurrence of postoperative anastomosis leakage was significantly higher in the High-SIS group than in the Low-SIS group (61.5% vs. 30.3%, p=0.021). Recently, we reported that postoperative anastomosis leakage was a significant prognostic factor for esophageal cancer patients (16). The respective 3- and 5-year OS rates were 63.9% and 53.2% in the non-anastomosis leakage group and 43.9% and 40.2% in the anastomosis leakage group (p=0.0049). Furthermore, Shoka et al. evaluated the clinical impact of SIS as a predictor of postoperative pneumonia in 1,415 gastric cancer patients who received gastrectomy (17). They found that the incidence of postoperative pneumonia was significantly higher in the SIS 2 group than in the SIS 0 or 1 group (p=0.001). Furthermore, a high SIS (SIS 2) was an independent risk factor for postoperative pneumonia (odds ratio=2.31, 95%CI=1.19-4.48, p=0.013). The incidences of overall postoperative surgical complications were significantly higher in the SIS 2 group (31.1%) than in the SIS 0 group (20.4%) or SIS 1 group (20.8%) (p=0.001). Therefore, the preoperative SIS status might be associated with the occurrence of postoperative surgical complications, and treatment strategies or postoperative management may need to be adjusted based on the preoperative SIS status.

There were some future suggestions in the present study. First, there was a clinical relationship between the SIS status and recurrence pattern. In the present study, the rate of hematological recurrence was significantly higher in the High-SIS group than in the Low-SIS group. Similar results were observed in previous studies (18-20). For example, Hara et al. evaluated the clinical impact of the SIS in 160 locally advanced gastric cancer patients (18) and found that hematological recurrence was significantly more frequent in the high-SIS group than in the low-SIS group (12.9% vs. 3.0%, p=0.028). In contrast, the frequency of local (3.2% vs. 1.5%, p=0.442), lymph node (9.7% vs. 6.0%, p=0.397), and peritoneal recurrence (18.3% vs. 14.9%, p=0.576) was not markedly different between the High- and Low-SIS groups. Kanda et al. also showed that the modified SIS (mSIS) was significantly associated with the prevalence of hematological recurrence (19). The incidence of hematological recurrence was 8.0% in mSIS 0, 19.2% in mSIS 1, and 21.1% in mSIS 2 (p=0.0425). However, the mechanism underlying the relationship between the SIS and hematological recurrence is unclear at present. Further studies should focus on this issue. Second, the optimal cut-off value of the SIS was unclear. In the present study, we set the cut-off value of SIS at 2 according to the 3- and 5-year OS rates. However, previous studies set the cut-off value of SIS at 1 according to the receiver operating characteristic curves (15, 21). To utilize the preoperative SIS for esophageal cancer treatment, it is necessary to set and the optimal cut-off value. A future study should focus on these issues.

In conclusion, the preoperative SIS affects the long-term oncological outcomes in esophageal cancer patients who receive curative treatment. Therefore, the perioperative SIS is a promising prognostic factor for esophageal cancer patients.

Footnotes

  • Authors’ Contributions

    TA and KK made substantial contributions to the concept and design. TA, MN, KS, SN, HS, KK, TY, IH, HC, MN, HT, TO, NY, TO and YR made substantial contributions to the acquisition of data and the analysis and interpretation of data. TA, HW, MN, HT, TO, NY and YR were involved in drafting the article or revising it critically for important intellectual content. TA, NM, KK and TO give their final approval of the version to be published.

  • Conflicts of Interest

    The Authors declare no conflicts of interest in association with the present study.

  • Received March 19, 2022.
  • Revision received March 31, 2022.
  • Accepted April 4, 2022.

References

  1. ↵
    1. Bray F,
    2. Ferlay J,
    3. Soerjomataram I,
    4. Siegel RL,
    5. Torre LA and
    6. Jemal A
    : Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6): 394-424, 2018. PMID: 30207593. DOI: 10.3322/caac.21492
    OpenUrlCrossRefPubMed
  2. ↵
    1. Torre LA,
    2. Bray F,
    3. Siegel RL,
    4. Ferlay J,
    5. Lortet-Tieulent J and
    6. Jemal A
    : Global cancer statistics, 2012. CA Cancer J Clin 65(2): 87-108, 2015. PMID: 25651787. DOI: 10.3322/caac.21262
    OpenUrlCrossRefPubMed
  3. ↵
    1. Muro K,
    2. Lordick F,
    3. Tsushima T,
    4. Pentheroudakis G,
    5. Baba E,
    6. Lu Z,
    7. Cho BC,
    8. Nor IM,
    9. Ng M,
    10. Chen LT,
    11. Kato K,
    12. Li J,
    13. Ryu MH,
    14. Zamaniah WIW,
    15. Yong WP,
    16. Yeh KH,
    17. Nakajima TE,
    18. Shitara K,
    19. Kawakami H,
    20. Narita Y,
    21. Yoshino T,
    22. Van Cutsem E,
    23. Martinelli E,
    24. Smyth EC,
    25. Arnold D,
    26. Minami H,
    27. Tabernero J and
    28. Douillard JY
    : Pan-Asian adapted ESMO Clinical Practice Guidelines for the management of patients with metastatic oesophageal cancer: a JSMO-ESMO initiative endorsed by CSCO, KSMO, MOS, SSO and TOS. Ann Oncol 30(1): 34-43, 2019. PMID: 30475943. DOI: 10.1093/annonc/mdy498
    OpenUrlCrossRefPubMed
  4. ↵
    1. Lordick F,
    2. Mariette C,
    3. Haustermans K,
    4. Obermannová R,
    5. Arnold D and ESMO Guidelines Committee
    : Oesophageal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 27(Suppl 5): v50-v57, 2016. PMID: 27664261. DOI: 10.1093/annonc/mdw329
    OpenUrlCrossRefPubMed
  5. ↵
    1. Atsumi Y,
    2. Kawahara S,
    3. Kakuta S,
    4. Onodera A,
    5. Hara K,
    6. Kazama K,
    7. Numata M,
    8. Aoyama T,
    9. Tamagawa A,
    10. Tamagawa H,
    11. Oshima T,
    12. Yukawa N and
    13. Rino Y
    : Low preoperative albumin-to-globulin ratio is a marker of poor prognosis in patients with esophageal cancer. In Vivo 35(6): 3555-3561, 2021. PMID: 34697194. DOI: 10.21873/invivo.12658
    OpenUrlAbstract/FREE Full Text
    1. Li S,
    2. Qiu R,
    3. Yuan G,
    4. Wang Q,
    5. Li Z,
    6. Li Q and
    7. Zhang N
    : Body composition in relation to postoperative anastomotic leakage and overall survival in patients with esophageal cancer. Nutrition 94: 111534, 2022. PMID: 34952360. DOI: 10.1016/j.nut.2021.111534
    OpenUrlCrossRefPubMed
    1. Wiwitkeyoonwong J,
    2. Jiarpinitnun C,
    3. Hiranyatheb P and
    4. Ngamphaiboon N
    : Impact of weight loss on patients with locally advanced esophageal and esophagogastric junction cancers treated with chemoradiotherapy. Asian Pac J Cancer Prev 22(12): 3847-3855, 2021. PMID: 34967563. DOI: 10.31557/APJCP.2021.22.12.3847
    OpenUrlCrossRefPubMed
  8. ↵
    1. Yoon JP,
    2. Nam JS,
    3. Abidin MFBZ,
    4. Kim SO,
    5. Lee EH,
    6. Choi IC and
    7. Chin JH
    : Comparison of preoperative nutritional indexes for outcomes after primary esophageal surgery for esophageal squamous cell carcinoma. Nutrients 13(11): 4086, 2021. PMID: 34836339. DOI: 10.3390/nu13114086
    OpenUrlCrossRefPubMed
  9. ↵
    1. Kuroda K,
    2. Toyokawa T,
    3. Miki Y,
    4. Yoshii M,
    5. Tamura T,
    6. Tanaka H,
    7. Lee S,
    8. Muguruma K,
    9. Yashiro M and
    10. Ohira M
    : Prognostic impact of postoperative systemic inflammatory response in patients with stage II/III gastric cancer. Sci Rep 12(1): 3025, 2022. PMID: 35194147. DOI: 10.1038/s41598-022-07098-3
    OpenUrlCrossRefPubMed
  10. ↵
    1. Qi Q,
    2. Song Q,
    3. Cheng Y and
    4. Wang N
    : Prognostic significance of preoperative prognostic nutritional index for overall survival and postoperative complications in esophageal cancer patients. Cancer Manag Res 13: 8585-8597, 2021. PMID: 34815713. DOI: 10.2147/CMAR.S333190
    OpenUrlCrossRefPubMed
  11. ↵
    1. Ma M,
    2. Weng M,
    3. Chen F,
    4. Hu Y,
    5. Lai J,
    6. Wang Y and
    7. Zhou Y
    : Systemic inflammation score is a prognostic marker after curative resection in gastric cancer. ANZ J Surg 89(4): 377-382, 2019. PMID: 30854753. DOI: 10.1111/ans.15103
    OpenUrlCrossRefPubMed
  12. ↵
    1. Colloca GA,
    2. Venturino A and
    3. Guarneri D
    : Systemic inflammation scores predict the activity of first-line chemotherapy in patients with metastatic pancreatic adenocarcinoma. Cancer Invest 39(1): 55-61, 2021. PMID: 33353411. DOI: 10.1080/07357907.2020.1863419
    OpenUrlCrossRefPubMed
  13. ↵
    1. Chang Y,
    2. An H,
    3. Xu L,
    4. Zhu Y,
    5. Yang Y,
    6. Lin Z and
    7. Xu J
    : Systemic inflammation score predicts postoperative prognosis of patients with clear-cell renal cell carcinoma. Br J Cancer 113(4): 626-633, 2015. PMID: 26135896. DOI: 10.1038/bjc.2015.241
    OpenUrlCrossRefPubMed
  14. ↵
    1. Nomoto D,
    2. Baba Y,
    3. Akiyama T,
    4. Okadome K,
    5. Iwatsuki M,
    6. Iwagami S,
    7. Miyamoto Y,
    8. Yoshida N,
    9. Watanabe M and
    10. Baba H
    : Adapted systemic inflammation score as a novel prognostic marker for esophageal squamous cell carcinoma patients. Ann Gastroenterol Surg 5(5): 669-676, 2021. PMID: 34585051. DOI: 10.1002/ags3.12464
    OpenUrlCrossRefPubMed
  15. ↵
    1. Fu X,
    2. Li T,
    3. Dai Y and
    4. Li J
    : Preoperative systemic inflammation score (SIS) is superior to neutrophil to lymphocyte ratio (NLR) as a predicting indicator in patients with esophageal squamous cell carcinoma. BMC Cancer 19(1): 721, 2019. PMID: 31331297. DOI: 10.1186/s12885-019-5940-6
    OpenUrlCrossRefPubMed
  16. ↵
    1. Aoyama T,
    2. Kazama K,
    3. Atsumi Y,
    4. Tamagawa H,
    5. Tamagawa A,
    6. Komori K,
    7. Machida D,
    8. Maezawa Y,
    9. Kano K,
    10. Hara K,
    11. Murakawa M,
    12. Numata M,
    13. Oshima T,
    14. Yukawa N,
    15. Masuda M and
    16. Rino Y
    : Clinical influence of anastomotic leakage on esophageal cancer survival and recurrence. Anticancer Res 40(1): 443-449, 2020. PMID: 31892599. DOI: 10.21873/anticanres.13972
    OpenUrlAbstract/FREE Full Text
  17. ↵
    1. Shoka M,
    2. Kanda M,
    3. Ito S,
    4. Mochizuki Y,
    5. Teramoto H,
    6. Ishigure K,
    7. Murai T,
    8. Asada T,
    9. Ishiyama A,
    10. Matsushita H,
    11. Tanaka C,
    12. Kobayashi D,
    13. Fujiwara M,
    14. Murotani K and
    15. Kodera Y
    : Systemic inflammation score as a predictor of pneumonia after radical resection of gastric cancer: analysis of a multi-institutional dataset. Dig Surg 37(5): 401-410, 2020. PMID: 32344400. DOI: 10.1159/000506940
    OpenUrlCrossRefPubMed
  18. ↵
    1. Hara K,
    2. Aoyama T,
    3. Yamada T,
    4. Nakazono M,
    5. Nagasawa S,
    6. Shimoda Y,
    7. Kumazu Y,
    8. Numata M,
    9. Hayashi T,
    10. Tamagawa H,
    11. Shiozawa M,
    12. Morinaga S,
    13. Yukawa N,
    14. Rino Y,
    15. Masuda M,
    16. Ogata T and
    17. Oshima T
    : The prognostic value of the perioperative systemic inflammation score for patients with advanced gastric cancer. Anticancer Res 40(3): 1503-1512, 2020. PMID: 32132050. DOI: 10.21873/anticanres.14095
    OpenUrlAbstract/FREE Full Text
  19. ↵
    1. Kanda M,
    2. Koike M,
    3. Tanaka C,
    4. Kobayashi D,
    5. Hattori N,
    6. Hayashi M,
    7. Yamada S,
    8. Omae K,
    9. Fujiwara M and
    10. Kodera Y
    : Modified systemic inflammation score is useful for risk stratification after radical resection of squamous cell carcinoma of the esophagus. Ann Surg Oncol 26(13): 4773-4781, 2019. PMID: 31605344. DOI: 10.1245/s10434-019-07914-7
    OpenUrlCrossRefPubMed
  20. ↵
    1. Sato B,
    2. Kanda M,
    3. Tanaka C,
    4. Kobayashi D,
    5. Iwata N,
    6. Hattori N,
    7. Suenaga M,
    8. Hayashi M,
    9. Yamada S,
    10. Murotani K,
    11. Fujiwara M and
    12. Kodera Y
    : Significance of preoperative systemic inflammation score in short-term and long-term outcomes of patients with pathological T2-4 gastric cancer after radical gastrectomy. World J Surg 42(10): 3277-3285, 2018. PMID: 29560531. DOI: 10.1007/s00268-018-4597-7
    OpenUrlCrossRefPubMed
  21. ↵
    1. Han L,
    2. Song Q,
    3. Jia Y,
    4. Chen X,
    5. Wang C,
    6. Chen P,
    7. Min R and
    8. Cheng Y
    : The clinical significance of systemic inflammation score in esophageal squamous cell carcinoma. Tumour Biol 37(3): 3081-3090, 2016. PMID: 26423404. DOI: 10.1007/s13277-015-4152-1
    OpenUrlCrossRefPubMed
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The Systemic Inflammation Score Is an Independent Prognostic Factor for Esophageal Cancer Patients who Receive Curative Treatment
TORU AOYAMA, MIHWA JU, KEISUKE KOMORI, HIROSHI TAMAGAWA, AYAKO TAMAGAWA, YUKIO MAEZAWA, ITARU HASHIMOTO, KAZUKI KANO, KENTARO HARA, HARUHIKO CHO, KENKI SEGAMI, DAISUKE MACHIDA, MASATO NAKAZONO, TAKASHI OSHIMA, NORIO YUKAWA, YASUSHI RINO
Anticancer Research May 2022, 42 (5) 2711-2717; DOI: 10.21873/anticanres.15749
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