Skip to main content

Main menu

  • Home
  • Current Issue
  • Archive
  • Info for
    • Authors
    • Editorial Policies
    • Subscribers
    • Advertisers
    • Editorial Board
    • Special Issues 2025
  • Journal Metrics
  • Other Publications
    • In Vivo
    • Cancer Genomics & Proteomics
    • Cancer Diagnosis & Prognosis
  • More
    • IIAR
    • Conferences
    • 2008 Nobel Laureates
  • About Us
    • General Policy
    • Contact
  • Other Publications
    • Anticancer Research
    • In Vivo
    • Cancer Genomics & Proteomics

User menu

  • Register
  • Subscribe
  • My alerts
  • Log in
  • My Cart

Search

  • Advanced search
Anticancer Research
  • Other Publications
    • Anticancer Research
    • In Vivo
    • Cancer Genomics & Proteomics
  • Register
  • Subscribe
  • My alerts
  • Log in
  • My Cart
Anticancer Research

Advanced Search

  • Home
  • Current Issue
  • Archive
  • Info for
    • Authors
    • Editorial Policies
    • Subscribers
    • Advertisers
    • Editorial Board
    • Special Issues 2025
  • Journal Metrics
  • Other Publications
    • In Vivo
    • Cancer Genomics & Proteomics
    • Cancer Diagnosis & Prognosis
  • More
    • IIAR
    • Conferences
    • 2008 Nobel Laureates
  • About Us
    • General Policy
    • Contact
  • Visit us on Facebook
  • Follow us on Linkedin
Research ArticleClinical Studies

Elevated Postoperative Levels of Serum C-reactive Protein Are Associated With Shorter Long-term Survival After Resection of Colorectal Liver Metastases, Regardless of the Occurrence of Infectious Complications

MASATSUNE SHIBUTANI, KENJIRO KIMURA, SHINICHIRO KASHIWAGI, EN WANG, YUKI OKAZAKI, KIYOSHI MAEDA, KOSEI HIRAKAWA and MASAICHI OHIRA
Anticancer Research May 2021, 41 (5) 2605-2610; DOI: https://doi.org/10.21873/anticanres.15040
MASATSUNE SHIBUTANI
1Department of Gastroenterological Surgery, Osaka City University Graduate School of Medicine, Osaka, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: fbxbj429@ybb.ne.jp
KENJIRO KIMURA
2Department of Department of Hepato-Biliary-Pancreatic Surgery, Osaka City University Graduate School of Medicine, Osaka, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
SHINICHIRO KASHIWAGI
3Department of Breast and Endocrine Surgery, Osaka City University Graduate School of Medicine, Osaka, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
EN WANG
1Department of Gastroenterological Surgery, Osaka City University Graduate School of Medicine, Osaka, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
YUKI OKAZAKI
1Department of Gastroenterological Surgery, Osaka City University Graduate School of Medicine, Osaka, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
KIYOSHI MAEDA
1Department of Gastroenterological Surgery, Osaka City University Graduate School of Medicine, Osaka, Japan;
4Department of Gastroenterological Surgery, Osaka City General Hospital, Osaka, Japan
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
KOSEI HIRAKAWA
1Department of Gastroenterological Surgery, Osaka City University Graduate School of Medicine, Osaka, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
MASAICHI OHIRA
1Department of Gastroenterological Surgery, Osaka City University Graduate School of Medicine, Osaka, Japan;
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

Abstract

Background/Aim: Recently, elevated levels of postoperative inflammatory markers have been reported to be associated with poorer long-term survival outcomes, regardless of the occurrence of infectious complications, in gastroenterological malignancies. The aim of this study was to evaluate the association between postoperative inflammation and shorter long-term survival after resection of colorectal liver metastases. Patients and Methods: A total of 104 patients who underwent R0 resection for colorectal liver metastases were enrolled. The CRPmax levels were defined as the highest postoperative serum C-reactive protein levels during hospital stay. Results: The high-CRPmax group had a significantly lower relapse-free survival rate than the low-CRPmax group, regardless of the occurrence of infectious complications. Conclusion: In colorectal liver metastasis as well as other malignancies, elevated postoperative levels of serum C-reactive protein are associated with shorter long-term survival, regardless of the occurrence of infectious complications.

Key Words:
  • Colorectal liver metastasis
  • inflammation
  • C-reactive protein
  • prognosis

In colorectal cancer, the liver is the most common site for synchronous distant metastasis and recurrence after curative surgery (1-3). Surgical resection is the only potentially curative therapeutic option and is accepted as the optimal treatment for colorectal liver metastases, providing 5-year survival rates of 37%-58% after complete resection (4-8). However, the incidence of postoperative complications, such as liver failure, bile leakage and intraabdominal abscess, remains high (9-12), although advances in surgical techniques and perioperative management contribute to decreased morbidity rates. Postoperative infectious complications have been reported to be associated with shorter long-term survival of patients with colorectal liver metastasis (13-16). This is because the increased production of inflammatory cytokines caused by infectious complications provides a favorable environment for the growth of micrometastases (17-21).

Recently, postoperative severe inflammation caused by excessive surgical stress as well as that induced by the postoperative infectious complications has been reported to be associated with shorter long-term survival in patients who undergo curative resection of the primary tumor in cases of gastroenterological malignancies, including gastric cancer and colorectal cancer (22, 23).

The present study evaluated whether or not elevated postoperative levels of serum C-reactive protein are associated with shorter long-term survival after resection of colorectal liver metastases, regardless of the occurrence of infectious complications.

Patients and Methods

Patients. A total of 104 patients who underwent R0 resection for colorectal liver metastases at Osaka City University Hospital between January 2001 and December 2017 were enrolled in this study. R0 resection was defined as no microscopic evidence of the tumor at or within 1 mm of the margin. Two cases of simultaneous multiple primary cancer were excluded from this study.

This retrospective study was approved by the Ethics Committee of Osaka City University (approval number: 4182) and conducted in accordance with the Declaration of Helsinki. All patients provided written informed consent.

Methods. Blood samples were taken for routine laboratory analysis of serum CRP levels at postoperative day (POD) 1, 3 and 7. In addition, blood tests were added or changed as needed according to the decision of the attending physician. The CRPmax levels were defined as the highest postoperative serum CRP levels during the hospital stay. An appropriate cut-off value of the CRPmax levels was determined according to a receiver operating characteristic (ROC) curve analysis. The patients were then classified into the low-CRPmax group and the high-CRPmax group, and the relationship between the CRPmax levels and the relapse-free survival was assessed.

Postoperative infectious complications include both surgical site infection and remote infection. Because patients without postoperative infectious complications were the main subjects in this study, the severity of the complications, such as Clavien-Dindo classification, was not evaluated.

Furthermore, we conducted a subgroup analysis limited to patients without postoperative infectious complications in order to evaluate the prognostic significance of the CRPmax levels independently of the presence or absence of postoperative infectious complications and to investigate the causes of an increased CRPmax levels other than infectious complications.

Statistical analyses. The relapse-free survival was defined as the interval between the date of operation and the date of the diagnosis of the first recurrence, death from any cause or last follow-up. The significance of differences in the CRPmax levels and the clinicopathological factors were analyzed using a chi-squared test, Fisher’s exact test and Mann-Whitney’s U-test. Survival curves were estimated using the Kaplan–Meier method, and the differences in the survival curves were assessed with the log-rank test. p-Values of <0.05 were considered to indicate statistical significance. All statistical analyses were performed using the SPSS software package for Windows (SPSS, Chicago, IL, USA).

Results

Patient characteristics. As shown in Table I, the study cohort included 55 male and 49 female patients, with a median age of 65.5 years old. Fifty-two patients had synchronous colorectal liver metastasis, and 52 had metachronous colorectal liver metastasis. Fifty-four patients had a single colorectal liver metastasis, and 50 had multiple colorectal liver metastases. The median diameter of the colorectal liver metastasis was 2.85 cm. The median amount of bleeding was 335 ml. The median operation time was 280.5 min. Thirteen (12.5%) patients developed postoperative infectious complications, including 18 surgical site infections and 3 remote infections (some had ≥2 infectious complications). The median duration of follow-up was 55.8 months. Seventy-two patients relapsed, and 50 patients died during the follow-up period. Patients who died within 30 days following hepatic resection were not included in this study.

View this table:
  • View inline
  • View popup
  • Download powerpoint
Table I.

Patient characteristics.

Classification and survival analysis according to CRPmax levels in all patients enrolled in this study. We used the CRPmax levels, which were a continuous variable, as the test variable and recurrence as the state variable. According to the ROC curve analysis of the CRPmax levels, 7.13 was adopted as the cut-off value (sensitivity: 72.6%, specificity: 54.8%) (Figure 1), and the patients were classified into the low- CRPmax group (n=37) and the high-CRPmax group (n=67) based on this value. The high-CRPmax group had a significantly lower relapse-free survival rate than the low- CRPmax group (p=0.0412) (Figure 2). Thirteen (12.5%) patients developed postoperative infectious complications. The median CRPmax levels of the patients with postoperative infectious complications were significantly higher than those of the patients without infectious complications (14.60 vs. 7.92) (p=0.001).

Figure 1.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 1.

A receiver operating characteristic curve analysis of CRPmax levels. Area under the curve=0.613; 95% Confidence Interval=0.490-0.737; p=0.068.

Figure 2.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 2.

Kaplan–Meier survival curve for the relapse-free survival according to the CRPmax levels. High CRPmax levels were associated with shorter relapse-free survival (p=0.0412).

Subgroup analyses limited to patients without postoperative infectious complications. Similarly, in a subgroup analysis limited to the patients without postoperative infectious complications, the high-CRPmax group had a significantly lower relapse-free survival rate than the low-CRPmax group (p=0.0372) (Figure 3).

Figure 3.
  • Download figure
  • Open in new tab
  • Download powerpoint
Figure 3.

Kaplan–Meier survival curve for relapse-free survival according to the CRPmax levels in patients without postoperative infectious complications. High CRPmax levels were associated with shorter relapse-free survival (p=0.0372).

The risk factors of elevated CRPmax levels after resection of colorectal liver metastasis were examined (Table II). Only large amount of bleeding (≥350 ml) was associated with a high CRPmax level (p=0.033).

View this table:
  • View inline
  • View popup
  • Download powerpoint
Table II.

Correlations between CRPmax levels and clinicopathological factors in patients without postoperative infectious complications.

Discussion

In this study, elevated postoperative levels of serum C-reactive protein were shown to be associated with shorter long-term survival after resection of colorectal liver metastases, regardless of the occurrence of infectious complications.

Infectious complications increase the levels of inflammatory cytokines, such as interleukin-6 (IL-6), and subsequent immunosuppression promotes the proliferation of occult micrometastases (19-21). This phenomenon is also caused by excessive surgical stress, even in patients without postoperative infectious complications. Postoperative infectious complications have been found to be associated with a worse prognosis of patients with various cancers (16, 24-26). However, the severity of complications has been relatively rarely considered, and even when it has been considered, only simple classification using the Clavien-Dindo classification system was performed (13-15). Furthermore, the types of complications have been rarely considered, although it has been reported that some types of infectious complications do not affect the prognosis (16). Therefore, the presence or absence of infectious complications alone is not sufficient for use as a predictor of the prognosis.

The serum CRP level is a comprehensive indicator that includes the degree of postoperative inflammation. In a recent report on the prognostic significance of postoperative serum CRP levels in patients with gastric cancer (22), it was concluded that postoperative CRP elevation was a better predictor than the occurrence of infectious complications. In the present study, elevated CRPmax levels were found to be associated with shorter long-term survival, independently of the presence or absence of postoperative complications in patients with colorectal liver metastasis. Therefore, strong postoperative inflammation adversely affects long-term survival regardless of the cause of inflammation.

Although it is widely recognized that an increase in intraoperative blood loss causes immunosuppression and subsequent deterioration of prognosis (27), the mechanism by which the amount of bleeding is associated with the CRPmax levels is unclear. A large amount of bleeding may indirectly indicate a surgical procedure with major invasion or bleeding itself may be the cause of increased inflammation.

Adjuvant chemotherapy after curative resection of colorectal liver metastases has been reported to be effective for treating patients with a high risk of recurrence (23, 28, 29). Therefore, risk classification based on CRPmax levels may help identify patients who are likely to benefit from adjuvant chemotherapy after curative resection of colorectal liver metastases.

To reduce postoperative inflammation, the following were important: (i) selection of a minimally invasive procedure, (ii) reduction of the amount of bleeding, (iii) reduction of postoperative infectious complications and (iv) appropriate response to complications.

Several limitations associated with the present study should be mentioned. First, the current study was a retrospective study of a small cohort in a single center. Second, although the serum CRP levels were routinely measured at POD 1, 3 and 7, the measurement of serum CRP levels was added or changed as needed according to the decision of the attending physician. Therefore, the days of blood tests were not always fixed. Third, we did not assess the overall survival in this study. This study included some patients who underwent resection of colorectal liver metastases 20 years ago. With the development of new cytotoxic and molecular-targeted therapies, the survival after recurrence has been significantly improved compared with 20 years ago. Therefore, we assessed only the relapse-free survival.

Conclusion

Elevated postoperative levels of serum C-reactive protein were revealed to be associated with shorter long-term survival after resection of colorectal liver metastases, regardless of the occurrence of infectious complications. Surgeons should minimize postoperative inflammation by reducing excessive surgical stress as well as performing strict postoperative management and reducing postoperative complications.

Footnotes

  • Authors’ Contributions

    MS designed the study, performed the statistical analysis and drafted the manuscript. KK, WE and YO collected the clinical data and revised the manuscript critically. SK, KM, KH and MO designed the study and critically reviewed the manuscript. All Authors read and approved the final manuscript.

  • Conflicts of Interest

    The Authors declare that they have no competing interests in regard to this study.

  • Received February 24, 2021.
  • Revision received April 4, 2021.
  • Accepted April 5, 2021.
  • Copyright © 2021 International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved.

References

  1. ↵
    1. van Gestel YR,
    2. de Hingh IH,
    3. van Herk-Sukel MP,
    4. van Erning FN,
    5. Beerepoot LV,
    6. Wijsman JH,
    7. Slooter GD,
    8. Rutten HJ,
    9. Creemers GJ and
    10. Lemmens VE
    : Patterns of metachronous metastases after curative treatment of colorectal cancer. Cancer Epidemiol 38(4): 448-454, 2014. PMID: 24841870. DOI: 10.1016/j.canep.2014.04.004
    OpenUrlCrossRefPubMed
    1. Riihimäki M,
    2. Hemminki A,
    3. Sundquist J and
    4. Hemminki K
    : Patterns of metastasis in colon and rectal cancer. Sci Rep 6: 29765, 2016. PMID: 27416752. DOI: 10.1038/srep29765
    OpenUrlCrossRefPubMed
  2. ↵
    1. Watanabe T,
    2. Muro K,
    3. Ajioka Y,
    4. Hashiguchi Y,
    5. Ito Y,
    6. Saito Y,
    7. Hamaguchi T,
    8. Ishida H,
    9. Ishiguro M,
    10. Ishihara S,
    11. Kanemitsu Y,
    12. Kawano H,
    13. Kinugasa Y,
    14. Kokudo N,
    15. Murofushi K,
    16. Nakajima T,
    17. Oka S,
    18. Sakai Y,
    19. Tsuji A,
    20. Uehara K,
    21. Ueno H,
    22. Yamazaki K,
    23. Yoshida M,
    24. Yoshino T,
    25. Boku N,
    26. Fujimori T,
    27. Itabashi M,
    28. Koinuma N,
    29. Morita T,
    30. Nishimura G,
    31. Sakata Y,
    32. Shimada Y,
    33. Takahashi K,
    34. Tanaka S,
    35. Tsuruta O,
    36. Yamaguchi T,
    37. Yamaguchi N,
    38. Tanaka T,
    39. Kotake K,
    40. Sugihara K and Japanese Society for Cancer of the Colon and Rectum
    : Japanese society for cancer of the colon and rectum (JSCCR) guidelines 2016 for the treatment of colorectal cancer. Int J Clin Oncol 23(1): 1-34, 2018. PMID: 28349281. DOI: 10.1007/s10147-017-1101-6
    OpenUrlCrossRefPubMed
  3. ↵
    1. Coppa GF,
    2. Eng K,
    3. Ranson JH,
    4. Gouge TH and
    5. Localio SA
    : Hepatic resection for metastatic colon and rectal cancer. An evaluation of preoperative and postoperative factors. Ann Surg 202(2): 203-208, 1985. PMID: 4015224. DOI: 10.1097/00000658-198508000-00010
    OpenUrlCrossRefPubMed
    1. Fong Y,
    2. Fortner J,
    3. Sun RL,
    4. Brennan MF and
    5. Blumgart LH
    : Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: Analysis of 1001 consecutive cases. Ann Surg 230(3): 309-18; discussion 318-21, 1999. PMID: 10493478. DOI: 10.1097/00000658-199909000-00004
    OpenUrlCrossRefPubMed
    1. Pawlik TM,
    2. Scoggins CR,
    3. Zorzi D,
    4. Abdalla EK,
    5. Andres A,
    6. Eng C,
    7. Curley SA,
    8. Loyer EM,
    9. Muratore A,
    10. Mentha G,
    11. Capussotti L and
    12. Vauthey JN
    : Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg 241(5): 715-22, discussion 722-4, 2005. PMID: 15849507. DOI: 10.1097/01.sla.0000160703.75808.7d
    OpenUrlCrossRefPubMed
    1. Are C,
    2. Gonen M,
    3. Zazzali K,
    4. Dematteo RP,
    5. Jarnagin WR,
    6. Fong Y,
    7. Blumgart LH and
    8. D’Angelica M
    : The impact of margins on outcome after hepatic resection for colorectal metastasis. Ann Surg 246(2): 295-300, 2007. PMID: 17667509. DOI: 10.1097/SLA.0b013e31811ea962
    OpenUrlCrossRefPubMed
  4. ↵
    1. Muratore A,
    2. Ribero D,
    3. Zimmitti G,
    4. Mellano A,
    5. Langella S and
    6. Capussotti L
    : Resection margin and recurrence-free survival after liver resection of colorectal metastases. Ann Surg Oncol 17(5): 1324-1329, 2010. PMID: 19847565. DOI: 10.1245/s10434-009-0770-4
    OpenUrlCrossRefPubMed
  5. ↵
    1. Jarnagin WR,
    2. Gonen M,
    3. Fong Y,
    4. DeMatteo RP,
    5. Ben-Porat L,
    6. Little S,
    7. Corvera C,
    8. Weber S and
    9. Blumgart LH
    : Improvement in perioperative outcome after hepatic resection: Analysis of 1,803 consecutive cases over the past decade. Ann Surg 236(4): 397-406; discussion 406-7, 2002. PMID: 12368667. DOI: 10.1097/01.SLA.0000029003.66466.B3
    OpenUrlCrossRefPubMed
    1. Laurent C,
    2. Sa Cunha A,
    3. Couderc P,
    4. Rullier E and
    5. Saric J
    : Influence of postoperative morbidity on long-term survival following liver resection for colorectal metastases. Br J Surg 90(9): 1131-1136, 2003. PMID: 12945082. DOI: 10.1002/bjs.4202
    OpenUrlCrossRefPubMed
    1. Virani S,
    2. Michaelson JS,
    3. Hutter MM,
    4. Lancaster RT,
    5. Warshaw AL,
    6. Henderson WG,
    7. Khuri SF and
    8. Tanabe KK
    : Morbidity and mortality after liver resection: Results of the patient safety in surgery study. J Am Coll Surg 204(6): 1284-1292, 2007. PMID: 17544086. DOI: 10.1016/j.jamcollsurg.2007.02.067
    OpenUrlCrossRefPubMed
  6. ↵
    1. Viganò L,
    2. Ferrero A,
    3. Lo Tesoriere R and
    4. Capussotti L
    : Liver surgery for colorectal metastases: results after 10 years of follow-up. Long-term survivors, late recurrences, and prognostic role of morbidity. Ann Surg Oncol 15(9): 2458-2464, 2008. PMID: 18463927. DOI: 10.1245/s10434-008-9935-9
    OpenUrlCrossRefPubMed
  7. ↵
    1. Fukami Y,
    2. Maeda A,
    3. Takayama Y,
    4. Takahashi T,
    5. Uji M and
    6. Kaneoka Y
    : Adverse oncological outcome of surgical site infection after liver resection for colorectal liver metastases. Surg Today 49(2): 170-175, 2019. PMID: 30225661. DOI: 10.1007/s00595-018-1715-y
    OpenUrlCrossRefPubMed
    1. Farid SG,
    2. Aldouri A,
    3. Morris-Stiff G,
    4. Khan AZ,
    5. Toogood GJ,
    6. Lodge JP and
    7. Prasad KR
    : Correlation between postoperative infective complications and long-term outcomes after hepatic resection for colorectal liver metastasis. Ann Surg 251(1): 91-100, 2010. PMID: 19858702. DOI: 10.1097/SLA.0b013e3181bfda3c
    OpenUrlCrossRefPubMed
  8. ↵
    1. Mavros MN,
    2. de Jong M,
    3. Dogeas E,
    4. Hyder O and
    5. Pawlik TM
    : Impact of complications on long-term survival after resection of colorectal liver metastases. Br J Surg 100(5): 711-718, 2013. PMID: 23364914. DOI: 10.1002/bjs.9060
    OpenUrlCrossRefPubMed
  9. ↵
    1. Matsuda A,
    2. Matsumoto S,
    3. Seya T,
    4. Matsutani T,
    5. Kishi T,
    6. Yokoi K,
    7. Wang P and
    8. Uchida E
    : Does postoperative complication have a negative impact on long-term outcomes following hepatic resection for colorectal liver metastasis? A meta-analysis. Ann Surg Oncol 20(8): 2485-2492, 2013. PMID: 23620215. DOI: 10.1245/s10434-013-2972-z
    OpenUrlCrossRefPubMed
  10. ↵
    1. Lundy J and
    2. Ford CM
    : Surgery, trauma and immune suppression. Evolving the mechanism. Ann Surg 197(4): 434-438, 1983. PMID: 6219640. DOI: 10.1097/00000658-198304000-00010
    OpenUrlCrossRefPubMed
    1. Horn F,
    2. Henze C and
    3. Heidrich K
    : Interleukin-6 signal transduction and lymphocyte function. Immunobiology 202(2): 151-167, 2000. PMID: 10993289. DOI: 10.1016/S0171-2985(00)80061-3
    OpenUrlCrossRefPubMed
  11. ↵
    1. Salvans S,
    2. Mayol X,
    3. Alonso S,
    4. Messeguer R,
    5. Pascual M,
    6. Mojal S,
    7. Grande L and
    8. Pera M
    : Postoperative peritoneal infection enhances migration and invasion capacities of tumor cells in vitro: An insight into the association between anastomotic leak and recurrence after surgery for colorectal cancer. Ann Surg 260(5): 939-43; discussion 943-4, 2014. PMID: 25243554. DOI: 10.1097/SLA.0000000000000958
    OpenUrlCrossRefPubMed
    1. Szczepanik AM,
    2. Scislo L,
    3. Scully T,
    4. Walewska E,
    5. Siedlar M,
    6. Kolodziejczyk P,
    7. Lenart M,
    8. Rutkowska M,
    9. Galas A,
    10. Czupryna A and
    11. Kulig J
    : IL-6 serum levels predict postoperative morbidity in gastric cancer patients. Gastric Cancer 14(3): 266-273, 2011. PMID: 21505767. DOI: 10.1007/s10120-011-0039-z
    OpenUrlCrossRefPubMed
  12. ↵
    1. Taniguchi Y,
    2. Kurokawa Y,
    3. Hagi T,
    4. Takahashi T,
    5. Miyazaki Y,
    6. Tanaka K,
    7. Makino T,
    8. Yamasaki M,
    9. Nakajima K,
    10. Mori M and
    11. Doki Y
    : Methylprednisolone inhibits tumor growth and peritoneal seeding induced by surgical stress and postoperative complications. Ann Surg Oncol 26(9): 2831-2838, 2019. PMID: 31286307. DOI: 10.1245/s10434-019-07585-4
    OpenUrlCrossRefPubMed
  13. ↵
    1. Kurokawa Y,
    2. Yamashita K,
    3. Kawabata R,
    4. Fujita J,
    5. Imamura H,
    6. Takeno A,
    7. Takahashi T,
    8. Yamasaki M,
    9. Eguchi H and
    10. Doki Y
    : Prognostic value of postoperative C-reactive protein elevation versus complication occurrence: A multicenter validation study. Gastric Cancer 23(5): 937-943, 2020. PMID: 32314097. DOI: 10.1007/s10120-020-01073-5
    OpenUrlCrossRefPubMed
  14. ↵
    1. Shibutani M,
    2. Nakao S,
    3. Maeda K,
    4. Nagahara H,
    5. Fukuoka T,
    6. Iseki Y,
    7. Hirakawa K and
    8. Ohira M
    : Inflammation caused by surgical stress has a negative impact on the long-term survival outcomes in patients with colorectal cancer. Anticancer Res 40(6): 3535-3542, 2020. PMID: 32487655. DOI: 10.21873/anticanres.14342
    OpenUrlAbstract/FREE Full Text
  15. ↵
    1. Artinyan A,
    2. Orcutt ST,
    3. Anaya DA,
    4. Richardson P,
    5. Chen GJ and
    6. Berger DH
    : Infectious postoperative complications decrease long-term survival in patients undergoing curative surgery for colorectal cancer: A study of 12,075 patients. Ann Surg 261(3): 497-505, 2015. PMID: 25185465. DOI: 10.1097/SLA.0000000000000854
    OpenUrlCrossRefPubMed
    1. Kataoka K,
    2. Takeuchi H,
    3. Mizusawa J,
    4. Igaki H,
    5. Ozawa S,
    6. Abe T,
    7. Nakamura K,
    8. Kato K,
    9. Ando N and
    10. Kitagawa Y
    : Prognostic impact of postoperative morbidity after esophagectomy for esophageal cancer: Exploratory analysis of JCOG9907. Ann Surg 265(6): 1152-1157, 2017. PMID: 27280509. DOI: 10.1097/SLA.0000000000001828
    OpenUrlCrossRefPubMed
  16. ↵
    1. Tokunaga M,
    2. Tanizawa Y,
    3. Bando E,
    4. Kawamura T and
    5. Terashima M
    : Poor survival rate in patients with postoperative intra-abdominal infectious complications following curative gastrectomy for gastric cancer. Ann Surg Oncol 20(5): 1575-1583, 2013. PMID: 23076557. DOI: 10.1245/s10434-012-2720-9
    OpenUrlCrossRefPubMed
  17. ↵
    1. Dhar DK,
    2. Kubota H,
    3. Tachibana M,
    4. Kotoh T,
    5. Tabara H,
    6. Watanabe R,
    7. Kohno H and
    8. Nagasue N
    : Long-term survival of transmural advanced gastric carcinoma following curative resection: Multivariate analysis of prognostic factors. World J Surg 24(5): 588-93; discussion 593-4, 2000. PMID: 10787082. DOI: 10.1007/s002689910099
    OpenUrlCrossRefPubMed
  18. ↵
    1. Hasegawa K,
    2. Saiura A,
    3. Takayama T,
    4. Miyagawa S,
    5. Yamamoto J,
    6. Ijichi M,
    7. Teruya M,
    8. Yoshimi F,
    9. Kawasaki S,
    10. Koyama H,
    11. Oba M,
    12. Takahashi M,
    13. Mizunuma N,
    14. Matsuyama Y,
    15. Watanabe T,
    16. Makuuchi M and
    17. Kokudo N
    : Adjuvant oral uracil-tegafur with leucovorin for colorectal cancer liver metastases: A randomized controlled trial. PLoS One 11(9): e0162400, 2016. PMID: 27588959. DOI: 10.1371/journal.pone.0162400
    OpenUrlCrossRefPubMed
  19. ↵
    1. Kobayashi S,
    2. Beppu T,
    3. Honda G,
    4. Yamamoto M,
    5. Takahashi K,
    6. Endo I,
    7. Hasegawa K,
    8. Kotake K,
    9. Itabashi M,
    10. Hashiguchi Y,
    11. Kotera Y,
    12. Sakamoto K,
    13. Yamaguchi T,
    14. Morita S,
    15. Tabuchi K,
    16. Miyazaki M and
    17. Sugihara K
    : Survival benefit of and indications for adjuvant chemotherapy for resected colorectal liver metastases-A Japanese nationwide survey. J Gastrointest Surg 24(6): 1244-1260, 2020. PMID: 31197683. DOI: 10.1007/s11605-019-04250-9
    OpenUrlCrossRefPubMed
PreviousNext
Back to top

In this issue

Anticancer Research: 41 (5)
Anticancer Research
Vol. 41, Issue 5
May 2021
  • Table of Contents
  • Table of Contents (PDF)
  • Index by author
  • Back Matter (PDF)
  • Ed Board (PDF)
  • Front Matter (PDF)
Print
Download PDF
Article Alerts
Sign In to Email Alerts with your Email Address
Email Article

Thank you for your interest in spreading the word on Anticancer Research.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Elevated Postoperative Levels of Serum C-reactive Protein Are Associated With Shorter Long-term Survival After Resection of Colorectal Liver Metastases, Regardless of the Occurrence of Infectious Complications
(Your Name) has sent you a message from Anticancer Research
(Your Name) thought you would like to see the Anticancer Research web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
7 + 11 =
Solve this simple math problem and enter the result. E.g. for 1+3, enter 4.
Citation Tools
Elevated Postoperative Levels of Serum C-reactive Protein Are Associated With Shorter Long-term Survival After Resection of Colorectal Liver Metastases, Regardless of the Occurrence of Infectious Complications
MASATSUNE SHIBUTANI, KENJIRO KIMURA, SHINICHIRO KASHIWAGI, EN WANG, YUKI OKAZAKI, KIYOSHI MAEDA, KOSEI HIRAKAWA, MASAICHI OHIRA
Anticancer Research May 2021, 41 (5) 2605-2610; DOI: 10.21873/anticanres.15040

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Reprints and Permissions
Share
Elevated Postoperative Levels of Serum C-reactive Protein Are Associated With Shorter Long-term Survival After Resection of Colorectal Liver Metastases, Regardless of the Occurrence of Infectious Complications
MASATSUNE SHIBUTANI, KENJIRO KIMURA, SHINICHIRO KASHIWAGI, EN WANG, YUKI OKAZAKI, KIYOSHI MAEDA, KOSEI HIRAKAWA, MASAICHI OHIRA
Anticancer Research May 2021, 41 (5) 2605-2610; DOI: 10.21873/anticanres.15040
Twitter logo Facebook logo Mendeley logo
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Jump to section

  • Article
    • Abstract
    • Patients and Methods
    • Results
    • Discussion
    • Conclusion
    • Footnotes
    • References
  • Figures & Data
  • Info & Metrics
  • PDF

Related Articles

  • No related articles found.
  • PubMed
  • Google Scholar

Cited By...

  • Impact of Intraoperative Blood Loss and Blood Transfusion on the Prognosis of Colorectal Liver Metastasis Following Curative Resection
  • The Impact of Intraoperative Blood Loss on the Survival After Laparoscopic Surgery for Colorectal Cancer
  • Google Scholar

More in this TOC Section

  • Feasibility of an Exercise Training Program Among Patients With Newly Diagnosed Advanced Breast Cancer
  • Impact of Surgery Refusal on Overall Survival in Merkel Cell Carcinoma
  • Association of County-level Social Determinants and Pancreatic Cancer Incidence in the United States
Show more Clinical Studies

Similar Articles

Keywords

  • colorectal liver metastasis
  • inflammation
  • c-reactive protein
  • prognosis
Anticancer Research

© 2025 Anticancer Research

Powered by HighWire