The utility of serum osteopontin levels for predicting postoperative complications after colorectal cancer surgery.


Journal

International journal of clinical oncology
ISSN: 1437-7772
Titre abrégé: Int J Clin Oncol
Pays: Japan
ID NLM: 9616295

Informations de publication

Date de publication:
Nov 2022
Historique:
received: 09 03 2022
accepted: 19 07 2022
pubmed: 12 8 2022
medline: 29 10 2022
entrez: 11 8 2022
Statut: ppublish

Résumé

Osteopontin (OPN) is a secretory glycoprotein, which is expressed not only in osteoblasts, but immune cells including macrophages and activated T cells. Its pleiotropic immune functions, such as bone remodeling, cancer progression, immune response, and inflammation have been reported previously. However, the association between OPN and postoperative complications (POC) after colorectal cancer (CRC) surgery has not been studied, so far. Peripheral blood samples were collected before (pre) and immediately after surgery (post), and on postoperative days (POD) 1, 3, 5, and 7. Serum OPN levels were measured by ELISA. In total, 78 patients who underwent elective CRC surgery were divided into the No-POC (n = 54) and POC (n = 24) groups. The POC group had significantly higher OPN levels than the No-POC group throughout the postoperative observation period. The maximum OPN levels from pre- to postsurgical samples showed the best predictive potential for POCs (cut off: 20.75 ng/mL, area under the curve: 0.724) and were correlated with length of postoperative stays. OPN values were significantly correlated with C-reactive protein on POD3 and were identified as an independent predictive marker for POCs (odds ratio: 3.88, 95% CI: 1.175-12.798, P = 0.026). The severity of POCs was reflected in increased OPN levels. Increased postoperative OPN was associated with increased postoperative inflammatory host responses and POC after CRC surgery. Serum OPN level may be a useful biomarker for early prediction of POC and it may provide additional information for treatment decisions to prevent POC.

Sections du résumé

BACKGROUND/AIM OBJECTIVE
Osteopontin (OPN) is a secretory glycoprotein, which is expressed not only in osteoblasts, but immune cells including macrophages and activated T cells. Its pleiotropic immune functions, such as bone remodeling, cancer progression, immune response, and inflammation have been reported previously. However, the association between OPN and postoperative complications (POC) after colorectal cancer (CRC) surgery has not been studied, so far.
METHODS METHODS
Peripheral blood samples were collected before (pre) and immediately after surgery (post), and on postoperative days (POD) 1, 3, 5, and 7. Serum OPN levels were measured by ELISA. In total, 78 patients who underwent elective CRC surgery were divided into the No-POC (n = 54) and POC (n = 24) groups.
RESULTS RESULTS
The POC group had significantly higher OPN levels than the No-POC group throughout the postoperative observation period. The maximum OPN levels from pre- to postsurgical samples showed the best predictive potential for POCs (cut off: 20.75 ng/mL, area under the curve: 0.724) and were correlated with length of postoperative stays. OPN values were significantly correlated with C-reactive protein on POD3 and were identified as an independent predictive marker for POCs (odds ratio: 3.88, 95% CI: 1.175-12.798, P = 0.026). The severity of POCs was reflected in increased OPN levels.
CONCLUSION CONCLUSIONS
Increased postoperative OPN was associated with increased postoperative inflammatory host responses and POC after CRC surgery. Serum OPN level may be a useful biomarker for early prediction of POC and it may provide additional information for treatment decisions to prevent POC.

Identifiants

pubmed: 35951171
doi: 10.1007/s10147-022-02225-6
pii: 10.1007/s10147-022-02225-6
doi:

Substances chimiques

Biomarkers 0
C-Reactive Protein 9007-41-4
Osteopontin 106441-73-0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1706-1716

Subventions

Organisme : Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan
ID : 15K10037

Informations de copyright

© 2022. The Author(s) under exclusive licence to Japan Society of Clinical Oncology.

Références

Arnold M, Sierra MS, Laversanne M et al (2017) Global patterns and trends in colorectal cancer incidence and mortality. Gut 66:683–691
doi: 10.1136/gutjnl-2015-310912 pubmed: 26818619
Torre LA, Siegel RL, Ward EM et al (2016) Global cancer incidence and mortality rates and trends–an update. Cancer Epidemiol Biomarkers Prev 25:16–27
doi: 10.1158/1055-9965.EPI-15-0578 pubmed: 26667886
Oliphant R, Nicholson GA, Horgan PG et al (2014) The impact of surgical specialisation on survival following elective colon cancer surgery. Int J Colorectal Dis 29:1143–1150
doi: 10.1007/s00384-014-1965-0 pubmed: 25034593
Alves A, Panis Y, Mathieu P et al (2005) Postoperative mortality and morbidity in French patients undergoing colorectal surgery: results of a prospective multicenter study. Arch Surg 140:278–283 (discussion 284)
doi: 10.1001/archsurg.140.3.278 pubmed: 15781793
Maruyama H, Kusachi S, Makino H et al (2020) Postoperative infection after colorectal surgery: subanalysis of data from the 2015 Japan postoperative infectious complications survey. J Nippon Med Sch 87:204–210
doi: 10.1272/jnms.JNMS.2020_87-403 pubmed: 32009069
McSorley ST, Watt DG, Horgan PG et al (2016) Postoperative systemic inflammatory response, complication severity, and survival following surgery for colorectal cancer. Ann Surg Oncol 23:2832–2840
doi: 10.1245/s10434-016-5204-5 pubmed: 27016295 pmcid: 4972846
Law WL, Choi HK, Lee YM et al (2007) The impact of postoperative complications on long-term outcomes following curative resection for colorectal cancer. Ann Surg Oncol 14:2559–2566
doi: 10.1245/s10434-007-9434-4 pubmed: 17522945
Miyamoto Y, Hiyoshi Y, Tokunaga R et al (2020) Postoperative complications are associated with poor survival outcome after curative resection for colorectal cancer: a propensity-score analysis. J Surg Oncol 122:344–349
doi: 10.1002/jso.25961 pubmed: 32346880
Wang KX, Denhardt DT (2008) Osteopontin: role in immune regulation and stress responses. Cytokine Growth Factor Rev 19:333–345
doi: 10.1016/j.cytogfr.2008.08.001 pubmed: 18952487
Cantor H, Shinohara ML (2009) Regulation of T-helper-cell lineage development by osteopontin: the inside story. Nat Rev Immunol 9:137–141
doi: 10.1038/nri2460 pubmed: 19096390 pmcid: 2696694
Lund SA, Giachelli CM, Scatena M (2009) The role of osteopontin in inflammatory processes. J Cell Commun Signal 3:311–322
doi: 10.1007/s12079-009-0068-0 pubmed: 19798593 pmcid: 2778587
Santamaria MH, Corral RS (2013) Osteopontin-dependent regulation of Th1 and Th17 cytokine responses in Trypanosoma cruzi-infected C57BL/6 mice. Cytokine 61:491–498
doi: 10.1016/j.cyto.2012.10.027 pubmed: 23199812
Hirano Y, Aziz M, Yang WL et al (2015) Neutralization of osteopontin attenuates neutrophil migration in sepsis-induced acute lung injury. Crit Care 19:53
doi: 10.1186/s13054-015-0782-3 pubmed: 25887405 pmcid: 4345018
Aziz MM, Ishihara S, Mishima Y et al (2009) MFG-E8 attenuates intestinal inflammation in murine experimental colitis by modulating osteopontin-dependent alphavbeta3 integrin signaling. J Immunol 182:7222–7232
doi: 10.4049/jimmunol.0803711 pubmed: 19454719
Cen C, Aziz M, Yang WL et al (2017) Osteopontin blockade attenuates renal injury after ischemia reperfusion by inhibiting NK cell infiltration. Shock 47:52–60
doi: 10.1097/SHK.0000000000000721 pubmed: 27504800 pmcid: 5167622
Dindo D, Demartines N, Clavien P-A (2004) Classification of surgical complications. Ann Surg 240:205–213
doi: 10.1097/01.sla.0000133083.54934.ae pubmed: 15273542 pmcid: 1360123
Jain S, Chakraborty G, Bulbule A et al (2007) Osteopontin: an emerging therapeutic target for anticancer therapy. Expert Opin Ther Targets 11:81–90
doi: 10.1517/14728222.11.1.81 pubmed: 17150036
Zhao H, Chen Q, Alam A et al (2018) The role of osteopontin in the progression of solid organ tumour. Cell Death Dis 9:356
doi: 10.1038/s41419-018-0391-6 pubmed: 29500465 pmcid: 5834520
Hattori T, Iwasaki-Hozumi H, Bai G et al (2021) Both full-length and protease-cleaved products of osteopontin are elevated in infectious diseases. Biomedicines 9(8):1006
doi: 10.3390/biomedicines9081006 pubmed: 34440210 pmcid: 8394573
Mishima R, Takeshima F, Sawai T et al (2007) High plasma osteopontin levels in patients with inflammatory bowel disease. J Clin Gastroenterol 41:167–172
doi: 10.1097/MCG.0b013e31802d6268 pubmed: 17245215
Scatena M, Liaw L, Giachelli CM (2007) Osteopontin: a multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler Thromb Vasc Biol 27:2302–2309
doi: 10.1161/ATVBAHA.107.144824 pubmed: 17717292
Menger MD, Vollmar B (2004) Surgical trauma: hyperinflammation versus immunosuppression? Langenbecks Arch Surg 389:475–484
doi: 10.1007/s00423-004-0472-0 pubmed: 15173946
Roumen RM, Hendriks T, van der Ven-Jongekrijg J et al (1993) Cytokine patterns in patients after major vascular surgery, hemorrhagic shock, and severe blunt trauma. Relation with subsequent adult respiratory distress syndrome and multiple organ failure. Ann Surg 218:769–776
doi: 10.1097/00000658-199312000-00011 pubmed: 8257227 pmcid: 1243073
Korner H, Nielsen HJ, Soreide JA et al (2009) Diagnostic accuracy of C-reactive protein for intraabdominal infections after colorectal resections. J Gastrointest Surg 13:1599–1606
doi: 10.1007/s11605-009-0928-1 pubmed: 19479312
Platt JJ, Ramanathan ML, Crosbie RA et al (2012) C-reactive protein as a predictor of postoperative infective complications after curative resection in patients with colorectal cancer. Ann Surg Oncol 19:4168–4177
doi: 10.1245/s10434-012-2498-9 pubmed: 22805866
Warschkow R, Tarantino I, Torzewski M et al (2011) Diagnostic accuracy of C-reactive protein and white blood cell counts in the early detection of inflammatory complications after open resection of colorectal cancer: a retrospective study of 1,187 patients. Int J Colorectal Dis 26:1405–1413
doi: 10.1007/s00384-011-1262-0 pubmed: 21701807
Cardinale F, Chinellato I, Caimmi S et al (2011) Perioperative period: immunological modifications. Int J Immunopathol Pharmacol 24:S3-12
doi: 10.1177/03946320110240S302 pubmed: 22014920
Lenz A, Franklin GA, Cheadle WG (2007) Systemic inflammation after trauma. Injury 38:1336–1345
doi: 10.1016/j.injury.2007.10.003 pubmed: 18048040
Zhang X, Tang M, Zhang Q et al (2021) The GLIM criteria as an effective tool for nutrition assessment and survival prediction in older adult cancer patients. Clin Nutr 40:1224–1232
doi: 10.1016/j.clnu.2020.08.004 pubmed: 32826109
van Kooten RT, Bahadoer RR, Peeters K et al (2021) Preoperative risk factors for major postoperative complications after complex gastrointestinal cancer surgery: a systematic review. Eur J Surg Oncol 47:3049–3058
doi: 10.1016/j.ejso.2021.07.021 pubmed: 34340874
van Kooten RT, Voeten DM, Steyerberg EW et al (2022) Patient-related prognostic factors for anastomotic leakage, major complications, and short-term mortality following esophagectomy for cancer: a systematic review and meta-analyses. Ann Surg Oncol 29:1358–1373
doi: 10.1245/s10434-021-10734-3 pubmed: 34482453
Morimoto J, Kon S, Matsui Y et al (2010) Osteopontin; as a target molecule for the treatment of inflammatory diseases. Curr Drug Targets 11:494–505
doi: 10.2174/138945010790980321 pubmed: 20196720
Shao Z, Morser J, Leung LLK (2014) Thrombin cleavage of osteopontin disrupts a pro-chemotactic sequence for dendritic cells, which is compensated by the release of its pro-chemotactic C-terminal fragment. J Biol Chem 289:27146–27158
doi: 10.1074/jbc.M114.572172 pubmed: 25112870 pmcid: 4175350
Agnihotri R, Crawford HC, Haro H et al (2001) Osteopontin, a novel substrate for matrix metalloproteinase-3 (stromelysin-1) and matrix metalloproteinase-7 (matrilysin). J Biol Chem 276:28261–28267
doi: 10.1074/jbc.M103608200 pubmed: 11375993
Ashkar S, Weber GF, Panoutsakopoulou V et al (2000) Eta-1 (osteopontin): an early component of type-1 (cell-mediated) immunity. Science 287:860–864
doi: 10.1126/science.287.5454.860 pubmed: 10657301
Chabas D, Baranzini SE, Mitchell D et al (2001) The influence of the proinflammatory cytokine, osteopontin, on autoimmune demyelinating disease. Science 294:1731–1735
doi: 10.1126/science.1062960 pubmed: 11721059
Da Silva AP, Pollett A, Rittling SR et al (2006) Exacerbated tissue destruction in DSS-induced acute colitis of OPN-null mice is associated with downregulation of TNF-alpha expression and non-programmed cell death. J Cell Physiol 208:629–639
doi: 10.1002/jcp.20701 pubmed: 16741956

Auteurs

Kumiko Sekiguchi (K)

Department of Surgery, Nippon Medical School Chiba Hokusoh Hospital, 1715 Kamagari , Inzai, Chiba, 270-1694, Japan.
Department of Surgery, Nippon Medical School Tama Nagayama Hospital, 1-7-1 Nagayama, Tama, Tokyo, 206-8512, Japan.

Akihisa Matsuda (A)

Department of Surgery, Nippon Medical School Chiba Hokusoh Hospital, 1715 Kamagari , Inzai, Chiba, 270-1694, Japan. a-matsu@nms.ac.jp.
Department of Gastrointestinal and Hepato-Biliary-Pancreatic Surgery, Nippon Medical School, 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8603, Japan. a-matsu@nms.ac.jp.

Marina Yamada (M)

Department of Surgery, Nippon Medical School Chiba Hokusoh Hospital, 1715 Kamagari , Inzai, Chiba, 270-1694, Japan.
Faculty of Medical Science, Nippon Sport Science University, 1221-1 Kamoshida-cho, Aoba-ku, Yokohama, Kanagawa, 227-0033, Japan.

Satoshi Matsumoto (S)

Department of Surgery, Nippon Medical School Chiba Hokusoh Hospital, 1715 Kamagari , Inzai, Chiba, 270-1694, Japan.

Nobuyuki Sakurazawa (N)

Department of Surgery, Nippon Medical School Chiba Hokusoh Hospital, 1715 Kamagari , Inzai, Chiba, 270-1694, Japan.
Department of Gastrointestinal and Hepato-Biliary-Pancreatic Surgery, Nippon Medical School, 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8603, Japan.

Youichi Kawano (Y)

Department of Surgery, Nippon Medical School Chiba Hokusoh Hospital, 1715 Kamagari , Inzai, Chiba, 270-1694, Japan.

Takeshi Yamada (T)

Department of Gastrointestinal and Hepato-Biliary-Pancreatic Surgery, Nippon Medical School, 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8603, Japan.

Masao Miyashita (M)

Department of Surgery, Nippon Medical School Chiba Hokusoh Hospital, 1715 Kamagari , Inzai, Chiba, 270-1694, Japan.

Hiroshi Yoshida (H)

Department of Gastrointestinal and Hepato-Biliary-Pancreatic Surgery, Nippon Medical School, 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8603, Japan.

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