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C-Reactive Protein and C-Reactive Protein-Based Scores to Predict Survival in Esophageal and Junctional Adenocarcinoma: Systematic Review and Meta-Analysis

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

Abstract

Background

Esophageal adenocarcinoma (EAC) has a poor prognosis; predictive markers of prognosis would facilitate advances in personalized therapy. C-reactive protein (CRP) and CRP-based scores are increasingly recommended across oncology; however, their role and value in EAC is unclear. This systematic review and meta-analysis examined CRP cut-point and scores and how they may best be applied in predicting survival in EAC.

Methods

A systematic literature search was conducted in EMBASE, Medline, Web of Science, Cochrane, Scopus and CINAHL databases, from inception to 1st October 2020. Studies reporting data from adults with EAC including adenocarcinoma of the gastro-esophageal junction (AEG), pre-treatment CRP or CRP-based score and Hazard Ratio (HR) for survival were included. QUIPS tool assessed risk of bias. Meta-analysis was undertaken.

Results

A total of 819 records were screened. Eight papers were included, with data for 1475 people. CRP cut-points ranged from 2.8 to 10 mg/L. The Glasgow Prognostic Score (GPS) and modified GPS were the most commonly reported scores. On meta-analysis, elevated preoperative GPS/mGPS was significantly associated with worse overall survival (hazards ratio [HR] 1.81, 95% confidence interval [CI] 1.25–2.62, p = 0.002); results were similar in subgroup analyses of multimodal treatment, M0 disease, and R0 resection.

Conclusions

This is the first review to evaluate comprehensively the evidence for CRP and CRP-based scores in EAC. Meta-analysis demonstrated that elevated preoperative GPS or mGPS was significantly associated with reduced overall survival in EAC, including AEG. There is insufficient evidence to support use of CRP alone. Future studies should examine GPS/mGPS in EAC prospectively, alone and combined with other prognostic markers.

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References

  1. Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021;71(3):209–49. https://doi.org/10.3322/caac.21660.

    Article  PubMed  Google Scholar 

  2. Integrated genomic characterization of oesophageal carcinoma. Nature. 2017;541(7636):169–75. https://doi.org/10.1038/nature20805.

    Article  CAS  Google Scholar 

  3. Cools-Lartigue J, Ferri L. Should multidisciplinary treatment differ for esophageal adenocarcinoma versus esophageal squamous cell cancer? Ann Surg Oncol. 2019;26(4):1014–27. https://doi.org/10.1245/s10434-019-07162-9.

    Article  PubMed  Google Scholar 

  4. Rice TW, Patil DT, Blackstone EH. 8th edition AJCC/UICC staging of cancers of the esophagus and esophagogastric junction: application to clinical practice. Ann Cardiothorac Surg. 2017;6(2):119–30. https://doi.org/10.21037/acs.2017.03.14.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Arnold M, Laversanne M, Brown LM, Devesa SS, Bray F. Predicting the future burden of esophageal cancer by histological subtype: international trends in incidence up to 2030. Am J Gastroenterol. 2017;112(8):1247–55. https://doi.org/10.1038/ajg.2017.155.

    Article  PubMed  Google Scholar 

  6. Griffin SM, Jones R, Kamarajah SK, et al. Evolution of esophagectomy for cancer over 30 years: changes in presentation, management and outcomes. Ann Surg Oncol. 2021;28(6):3011–22. https://doi.org/10.1245/s10434-020-09200-3.

    Article  PubMed  Google Scholar 

  7. Jomrich G, Paireder M, Gleiss A, Kristo I, Harpain L, Schoppmann SF. Comparison of inflammation-based prognostic scores in a cohort of patients with resectable esophageal cancer. Gastroenterol Res Pract. 2017. https://doi.org/10.1155/2017/1678584.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis. 2009;30(7):1073–81. https://doi.org/10.1093/carcin/bgp127.

    Article  CAS  PubMed  Google Scholar 

  9. Black S, Kushner I, Samols D. C-reactive protein. J Biol Chem. 2004;279(47):48487–90. https://doi.org/10.1074/jbc.R400025200.

    Article  CAS  PubMed  Google Scholar 

  10. Shrotriya S, Walsh D, Bennani-Baiti N, Thomas S, Lorton C. C-reactive protein is an important biomarker for prognosis tumor recurrence and treatment response in adult solid tumors: a systematic review. PLoS One. 2015;10(12):e0143080. https://doi.org/10.1371/journal.pone.0143080.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Valdes M, Chasen MR. Tumour inflammatory response: adding fuel to the fire? Curr Oncol. 2015;22(1):7–9. https://doi.org/10.3747/co.22.2303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Dolan RD, Lim J, McSorley ST, Horgan PG, McMillan DC. The role of the systemic inflammatory response in predicting outcomes in patients with operable cancer: systematic review and meta-analysis. Sci Rep. 2017;7(1):16717. https://doi.org/10.1038/s41598-017-16955-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Riley RD, Moons KGM, Snell KIE, et al. A guide to systematic review and meta-analysis of prognostic factor studies. BMJ. 2019;364:k4597. https://doi.org/10.1136/bmj.k4597.

    Article  PubMed  Google Scholar 

  14. Wang Y, Li P, Li J, et al. The prognostic value of pretreatment Glasgow Prognostic Score in patients with esophageal cancer: a meta-analysis [Review]. Cancer Manag Res. 2019;11:8181–90. https://doi.org/10.2147/CMAR.S203425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Huang Y, Feng JF, Liu JS, Chen QX. Prognostic role of serum C-reactive protein in esophageal cancer: a systematic review and meta-analysis [Review]. Therap Clin Risk Manag. 2015;11:89–94.

    Article  Google Scholar 

  16. Zingg U, Forberger J, Rajcic B, Langton C, Jamieson GG. Association of C-reactive protein levels and long-term survival after neoadjuvant therapy and esophagectomy for esophageal cancer. J Gastrointest Surg. 2010;14(3):462–9. https://doi.org/10.1007/s11605-009-1113-2.

    Article  PubMed  Google Scholar 

  17. Jagadesham VP, Lagarde SM, Immanuel A, Griffin SM. Systemic inflammatory markers and outcome in patients with locally advanced adenocarcinoma of the oesophagus and gastro-oesophageal junction. Br J Surg. 2017;104(4):401–7. https://doi.org/10.1002/bjs.10425.

    Article  CAS  PubMed  Google Scholar 

  18. Zhang Y, Xiao G, Wang R. Clinical significance of systemic immuneinflammation index (SII) and C-reactive proteinto- albumin ratio (CAR) in patients with esophageal cancer: a meta-analysis. Cancer Manag Res. 2019;11:4185–200. https://doi.org/10.2147/CMAR.S190006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. https://doi.org/10.1136/bmj.n71.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med. 1998;17(24):2815–34. https://doi.org/10.1002/(sici)1097-0258(19981230)17:24%3c2815::aid-sim110%3e3.0.co;2-8.

    Article  CAS  PubMed  Google Scholar 

  21. Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials. 2007;8:16. https://doi.org/10.1186/1745-6215-8-16.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Hayden JA, van der Windt DA, Cartwright JL, Cote P, Bombardier C. Assessing bias in studies of prognostic factors. Ann Intern Med. 2013;158(4):280–6. https://doi.org/10.7326/0003-4819-158-4-201302190-00009.

    Article  PubMed  Google Scholar 

  23. Sterne JA, Sutton AJ, Ioannidis JP, et al. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ. 2011;343:d4002. https://doi.org/10.1136/bmj.d4002.

    Article  PubMed  Google Scholar 

  24. Jomrich G, Hollenstein M, John M, et al. The modified Glasgow Prognostic score is an independent prognostic indicator in neoadjuvantly treated adenocarcinoma of the esophagogastric junction. Oncotarget. 2018;9(6):6968–76. https://doi.org/10.18632/oncotarget.24087.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Dutta S, Going JJ, Crumley ABC, et al. The relationship between tumour necrosis, tumour proliferation, local and systemic inflammation, microvessel density and survival in patients undergoing potentially curative resection of oesophageal adenocarcinoma. Br J Cancer. 2012;106(4):702–10. https://doi.org/10.1038/bjc.2011.610.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Anciaux M, Van Gossum A, Wenglinski C, et al. Fat density is a novel prognostic marker in patients with esophageal cancer. Clin Nutr ESPEN. 2020;39:124–30. https://doi.org/10.1016/j.clnesp.2020.07.007.

    Article  PubMed  Google Scholar 

  27. Powell A, Eley C, Chin C, Coxon AH, Christian A, Lewis WG. Prognostic significance of serum inflammatory markers in esophageal cancer. Esophagus. 2021;18(2):267–77. https://doi.org/10.1007/s10388-020-00772-3.

    Article  PubMed  Google Scholar 

  28. Vashist YK, Loos J, Dedow J, et al. Glasgow Prognostic Score is a predictor of perioperative and long-term outcome in patients with only surgically treated esophageal cancer. Ann Surg Oncol. 2011;18(4):1130–8. https://doi.org/10.1245/s10434-010-1383-7.

    Article  PubMed  Google Scholar 

  29. Walsh SM, Casey S, Kennedy R, Ravi N, Reynolds JV. Does the modified Glasgow Prognostic Score (mGPS) have a prognostic role in esophageal cancer? J Surg Oncol. 2016;113(7):732–7. https://doi.org/10.1002/jso.24225.

    Article  PubMed  Google Scholar 

  30. Wen J, Bedford M, Begum R, et al. The value of inflammation based prognostic scores in patients undergoing surgical resection for oesophageal and gastric carcinoma. J Surg Oncol. 2018;117(8):1697–707. https://doi.org/10.1002/jso.25057.

    Article  PubMed  Google Scholar 

  31. Lindenmann J, Fink-Neuboeck N, Avian A, et al. Preoperative Glasgow Prognostic Score as additional independent prognostic parameter for patients with esophageal cancer after curative esophagectomy. Eur J Surg Oncol. 2017;43(2):445–53. https://doi.org/10.1016/j.ejso.2016.10.015.

    Article  CAS  PubMed  Google Scholar 

  32. Zheng TL, Cao K, Liang C, et al. Prognostic value of C-reactive protein in esophageal cancer: a meta-analysis. Asian Pacific J Cancer Prev. 2014;15(19):8075–81.

    Article  Google Scholar 

  33. Bouwmeester W, Zuithoff NP, Mallett S, et al. Reporting and methods in clinical prediction research: a systematic review. PLoS Med. 2012;9(5):1–12. https://doi.org/10.1371/journal.pmed.1001221.

    Article  PubMed  Google Scholar 

  34. Kudou K, Nakashima Y, Haruta Y, et al. Comparison of inflammation-based prognostic scores associated with the prognostic impact of adenocarcinoma of esophagogastric junction and upper gastric cancer. Ann Surg Oncol. 2021;28:2059–67. https://doi.org/10.1245/s10434-020-08821-y.

  35. Wu J, Tan W, Chen L, Huang Z, Mai S. Clinicopathologic and prognostic significance of C-reactive protein/albumin ratio in patients with solid tumors: an updated systemic review and meta-analysis. Oncotarget. 2018;9(17):13934–47. https://doi.org/10.18632/oncotarget.24172.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Liu Z, Shi H, Chen L. Prognostic role of pre-treatment C-reactive protein/albumin ratio in esophageal cancer: a meta-analysis. BMC Cancer. 2019. https://doi.org/10.1186/s12885-019-6373-y.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Wang Y, Hu X, Huang Y, et al. Prognostic value of the C-reactive protein to albumin ratio in esophageal cancer: a systematic review and meta-analysis. Kaohsiung J Med Sci. 2020;36(1):54–61. https://doi.org/10.1002/kjm2.12129.

    Article  CAS  PubMed  Google Scholar 

  38. Dissemination CfRa. Systematic Reviews: CRD's guidance for undertaking reviews in health care. 2008. https://www.york.ac.uk/media/crd/Systematic_Reviews.pdf

  39. Matsunaga T, Miyata H, Sugimura K, et al. Prognostic significance of c-reactive protein-to-prealbumin ratio in patients with esophageal cancer. Yonago Acta Med. 2020;63(1):8–19. https://doi.org/10.33160/yam.2020.02.002.

    Article  CAS  PubMed  Google Scholar 

  40. Nakamura M, Iwahashi M, Nakamori M, et al. A new prognostic score for the survival of patients with esophageal squamous cell carcinoma. Surg Today. 2014;44(5):875–83. https://doi.org/10.1007/s00595-013-0628-z.

    Article  CAS  PubMed  Google Scholar 

  41. Chen P, Fang M, Wan Q, Zhang X, Song T, Wu S. High-sensitivity modified Glasgow prognostic score (HS-mGPS) Is superior to the mGPS in esophageal cancer patients treated with chemoradiotherapy. Oncotarget. 2017;8(59):99861–70. https://doi.org/10.18632/oncotarget.21734.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Tian R, Zhang F, Sun P, et al. The preoperative sensitive-modified Glasgow prognostic score is superior to the modified Glasgow prognostic score in predicting long-term survival for esophageal squamous cell carcinoma. Oncotarget. 2016;7(41):67485–94. https://doi.org/10.18632/oncotarget.11268.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Kouzu K, Tsujimoto H, Sugasawa H, et al. Modified geriatric nutrition risk index as a prognostic predictor of esophageal cancer. Esophagus. 2021;18(2):278–87. https://doi.org/10.1007/s10388-020-00795-w.

    Article  PubMed  Google Scholar 

  44. Noble F, Curtis N, Harris S, et al. Risk assessment using a novel score to predict anastomotic leak and major complications after oesophageal resection. J Gastrointest Surg. 2012;16(6):1083–95. https://doi.org/10.1007/s11605-012-1867-9.

    Article  PubMed  Google Scholar 

  45. Liesenfeld LF, Sauer P, Diener MK, et al. Prognostic value of inflammatory markers for detecting anastomotic leakage after esophageal resection. BMC Surg. 2020;20(1):324. https://doi.org/10.1186/s12893-020-00995-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Dutta S, Fullarton GM, Forshaw MJ, Horgan PG, McMillan DC. Persistent elevation of C-reactive protein following esophagogastric cancer resection as a predictor of postoperative surgical site infectious complications. World J Surg. 2011;35(5):1017–25. https://doi.org/10.1007/s00268-011-1002-1.

    Article  PubMed  Google Scholar 

  47. Lindenmann J, Fink-Neuboeck N, Koesslbacher M, et al. The influence of elevated levels of C-reactive protein and hypoalbuminemia on survival in patients with advanced inoperable esophageal cancer undergoing palliative treatment. J Surg Oncol. 2014;110(6):645–50. https://doi.org/10.1002/jso.23711.

    Article  CAS  PubMed  Google Scholar 

  48. Driver RJ, Handforth C, Radhakrishna G, Bennett MI, Ford AC, Everett SM. The Glasgow Prognostic Score at the time of palliative esophageal stent insertion is a predictive factor of 30-day mortality and overall survival. J Clin Gastroenterol. 2018;52(3):223–8. https://doi.org/10.1097/MCG.0000000000000773.

    Article  PubMed  Google Scholar 

  49. Reeh M, Ghadban T, Uzunoglu FG, et al. Hamburg-Glasgow classification: preoperative staging by combination of disseminated tumour load and systemic inflammation in oesophageal carcinoma. Br J Cancer. 2017;117(5):612–8. https://doi.org/10.1038/bjc.2017.219.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. McSorley ST, Lau HYN, McIntosh D, Forshaw MJ, McMillan DC, Crumley AB. Staging the tumor and staging the host: pretreatment combined neutrophil lymphocyte ratio and modified Glasgow Prognostic Score is associated with overall survival in patients with esophagogastric cancers undergoing treatment with curative intent. Ann Surg Oncol. 2021;28(2):722–31. https://doi.org/10.1245/s10434-020-09074-5.

    Article  PubMed  Google Scholar 

  51. Hart PC, Rajab IM, Alebraheem M, Potempa LA. C-reactive protein and cancer-diagnostic and therapeutic insights. Front Immunol. 2020;11:595835. https://doi.org/10.3389/fimmu.2020.595835.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Abbass T, Dolan RD, Laird BJ, McMillan DC. The relationship between imaging-based body composition analysis and the systemic inflammatory response in patients with cancer: a systematic review. Cancers (Basel). 2019. https://doi.org/10.3390/cancers11091304.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Joglekar S, Nau PN, Mezhir JJ. The impact of sarcopenia on survival and complications in surgical oncology: a review of the current literature. J Surg Oncol. 2015;112(5):503–9. https://doi.org/10.1002/jso.24025.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Dijksterhuis WPM, Latenstein AEJ, van Kleef JJ, et al. Cachexia and dietetic interventions in patients with esophagogastric cancer: a multicenter cohort study. J Natl Compr Canc Netw. 2021. https://doi.org/10.6004/jnccn.2020.7615.

    Article  PubMed  Google Scholar 

  55. Altman DG, Vergouwe Y, Royston P, Moons KGM. Prognosis and prognostic research: validating a prognostic model. BMJ. 2009;338:b605. https://doi.org/10.1136/bmj.b605.

    Article  PubMed  Google Scholar 

  56. Kyzas PA, Denaxa-Kyza D, Ioannidis JP. Quality of reporting of cancer prognostic marker studies: association with reported prognostic effect. J Natl Cancer Inst. 2007;99(3):236–43. https://doi.org/10.1093/jnci/djk032.

    Article  PubMed  Google Scholar 

  57. McShane LM, Altman DG, Sauerbrei W, et al. REporting recommendations for tumour MARKer prognostic studies (REMARK). Br J Cancer. 2005;93(4):387–91. https://doi.org/10.1038/sj.bjc.6602678.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Li M-X, Bi X-Y, Li Z-Y, et al. Prognostic role of Glasgow Prognostic Score in patients with hepatocellular carcinoma: a systematic review and meta-analysis. Medicine. 2015;94(49):e2133. https://doi.org/10.1097/MD.0000000000002133.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Altman DG. Categorising continuous variables. Br J Cancer. 1991;64(5):975. https://doi.org/10.1038/bjc.1991.441.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors thank Dr. Lina Zgaga, Dr. Noel Donlon, Dr. Ciarán Kenny, and Ms. Ailín Rogers for their helpful advice. Sincere thanks also to the research teams at Academic Department of Palliative Medicine, Our Lady’s Hospice & Care Services and Department of Surgery in Trinity Translational Medicine Institute for all their support in the conduct of the research.

Funding

No funding support was obtained for this study. Template forms and collected data are available on request from the corresponding author.

Author information

Authors and Affiliations

  1. Academic Department of Palliative Medicine, Our Lady’s Hospice & Care Services, Dublin, Ireland

    Cliona M. Lorton MB

  2. School of Medicine, Trinity College Dublin, Dublin, Ireland

    Cliona M. Lorton MB, Claire Donohoe MB, Jim O’Connell MD, John V. Reynolds MA & Joanne Lysaght PhD

  3. Cancer Immunology and Immunotherapy Group, Department of Surgery, Trinity Translational Medicine Institute, Trinity St. James’s Cancer Institute, Trinity College Dublin and St. James’s Hospital, Dublin, Ireland

    Cliona M. Lorton MB & Joanne Lysaght PhD

  4. Health Products Regulatory Authority, Dublin, Ireland

    Larissa Higgins MB

  5. Department of Oncology, St James’s Hospital, Dublin, Ireland

    Niamh O’Donoghue MB

  6. Gastro-intestinal Medicine and Surgery, St. James’s Hospital, Dublin, Ireland

    Claire Donohoe MB, Jim O’Connell MD & John V. Reynolds MA

  7. Department of Surgery, Trinity College Dublin, St James’s Hospital, Dublin, Ireland

    Claire Donohoe MB & John V. Reynolds MA

  8. John Stearne Medical Library, Trinity Centre for the Health Sciences, St James’s Hospital, Dublin, Ireland

    David Mockler BSc

  9. Department of Supportive Oncology, Levine Cancer Institute, Charlotte, NC, USA

    Declan Walsh MD

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Supplementary file 1.

Supplementary file 2.

10434_2021_10988_MOESM3_ESM.docx

Supplementary file 3. Supplementary Fig. 1 Subgroup analyses of clinical characteristics. Forest plot of hazard ratios for overall survival in EAC, including AEG, classified by GPS/mGPS; studies included surgery (a) and chemotherapy (b) R0-R2 resection status

10434_2021_10988_MOESM4_ESM.docx

Supplementary file 4. Supplementary Fig. 2 Subgroup analysis of study characteristics. Forest plot of hazard ratios for overall survival in EAC, including AEG, classified by GPS/mGPS for studies conducted in the United Kingdom or Ireland

Appendix 1

Appendix 1

EMBASE

  1. 1.

    'esophagus tumor'/exp

  2. 2.

    ‘Esophageal adenocarcinoma’/exp

  3. 3.

    ‘Esophagus carcinoma’/exp

  4. 4.

    ‘Esophagus cancer’/exp

  5. 5.

    (esophag* NEAR/3 (cancer* OR neoplasm* OR tumor? OR tumour? OR adenocarcinoma* OR carcinoma*)):ab,ti

  6. 6.

    (oesophag* NEAR/3 (cancer* OR neoplasm* OR tumor? OR tumour? OR adenocarcinoma* OR carcinoma*)):ab,ti

  7. 7.

    #1 OR #2 OR #3 OR #4 OR #5 OR #6

  8. 8.

    'c reactive protein'/exp

  9. 9.

    ('c-reactive protein' OR CRP OR 'creactive protein'):ti,ab

  10. 10.

    'glasgow prognostic score'/exp OR 'modified glasgow prognostic score'/exp

  11. 11.

    ('glasgow prognostic score' OR GPS OR 'modified glasgow prognostic score' OR mGPS):ti,ab

  12. 12.

    ((‘C- reactive protein’ OR CRP) NEAR/2 (albumin OR ALB)):ti,ab

  13. 13.

    (‘CRP/albumin ratio’ OR ‘CRP/ALB’):ti,ab

  14. 14.

    #8 OR #9 OR #10 OR #11 OR #12 OR #13

  15. 15.

    #7 AND #14

Medline

  1. 1.

    Esophageal Neoplasms/

  2. 2.

    (esophag* adj3 (cancer* OR neoplasm* OR tumor? OR tumour? OR adenocarcinoma* OR carcinoma)).ti,ab.

  3. 3.

    (oesophag* adj3 (cancer* OR neoplasm* OR tumor? OR tumour? OR adenocarcinoma* OR carcinoma*)).ti,ab.

  4. 4.

    or/1-3

  5. 5.

    C-Reactive Protein/

  6. 6.

    (c-reactive protein OR CRP OR creactive protein).ti,ab.

  7. 7.

    (glasgow prognostic score OR GPS OR modified glasgow prognostic score OR mGPS).ti,ab.

  8. 8.

    ((C- reactive protein OR CRP OR creactive protein) adj2 (albumin OR ALB)).ti,ab.

  9. 9.

    (CRP albumin ratio OR CRP ALB).ti,ab.

  10. 10.

    or/5-9

  11. 11.

    4 AND 10

CINAHL

  1. 1.

    (MH "Esophageal Neoplasms")

  2. 2.

    TI (esophag* N3 (cancer OR neoplasm*OR adenocarcinoma* OR tumo?r* OR carcinoma*)) OR AB (esophag* N3 (cancer OR neoplasm*OR adenocarcinoma* OR tumo?r* OR carcinoma*))

  3. 3.

    TI (oesophag* N3 (cancer OR neoplasm*OR adenocarcinoma* OR tumo?r* OR carcinoma*)) OR AB (oesophag* N3 (cancer OR neoplasm*OR adenocarcinoma* OR tumo?r* OR carcinoma*))

  4. 4.

    S1 OR S2 OR S3

  5. 5.

    MH "C-Reactive Protein"

  6. 6.

    TI (“C-Reactive Protein” OR “C Reactive Protein” OR “creactive protein”) OR AB (“C-Reactive Protein” OR “C Reactive Protein” OR “creactive protein” )

  7. 7.

    TI (“glasgow prognostic score” OR GPS OR “modified glasgow prognostic score” OR mGPS) OR AB (“glasgow prognostic score” OR GPS OR “modified glasgow prognostic score” OR mGPS)

  8. 8.

    TI ((‘C- reactive protein’ OR CRP OR “creactive protein”) N2 (albumin OR ALB)) OR AB ((‘C- reactive protein’ OR CRP OR “creactive protein”) N2 (albumin OR ALB))

  9. 9.

    TI (“CRP albumin ratio” OR “CRP ALB”) OR AB ((‘C- reactive protein’ OR CRP OR “creactive protein”) N2 (albumin OR ALB))

  10. 10.

    S5 OR S6 OR S7 OR S8 OR S9

  11. 11.

    S4 AND S10

Web of Science

TS =(((esophag* NEAR/2 (cancer* OR neoplasm* OR tumor? OR tumour? OR adenocarcinoma* OR carcinoma*)) OR (oesophag* NEAR/2 (cancer* OR neoplasm* OR tumor? OR tumour? OR adenocarcinoma* OR carcinoma*))) AND ((“c-reactive protein” OR CRP OR “creactive protein”) OR (“glasgow prognostic score” OR GPS OR “modified glasgow prognostic score” OR mGPS) OR ((“C- reactive protein” OR CRP) NEAR/2 (albumin OR ALB)) OR (“CRP albumin ratio” OR “CRP ALB”)))

Cochrane Library

  1. 1.

    [mh“Esophageal Neoplasms”]

  2. 2.

    (esophag* NEAR/3 (cancer OR neoplasm* OR tumor* OR tumour* OR adenocarcinoma* OR carcinoma*)):ti,ab,kw

  3. 3.

    (oesophag* NEAR/3 (cancer OR neoplasm* OR tumor* OR tumour OR adenocarcinoma* OR carcinoma*)):ti,ab,kw

  4. 4.

    #1 or #2 or #3

  5. 5.

    [mh”C-Reactive Protein”]

  6. 6.

    (“c-reactive protein” OR “c reactive protein” OR CRP OR “creactive protein”):ti,ab,kw

  7. 7.

    (“glasgow prognostic score” OR GPS OR “modified glasgow prognostic score” OR mGPS):ti,ab,kw

  8. 8.

    ((“C- reactive protein” OR CRP OR “creactive protein”) NEAR/2 (albumin OR ALB)):ti,ab,kw

  9. 9.

    (“CRP albumin ratio” OR “CRP ALB”):ti,ab,kw

  10. 10.

    #5 OR #6 OR #7 OR #8 OR #9

  11. 11.

    #4 AND #10

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Lorton, C.M., Higgins, L., O’Donoghue, N. et al. C-Reactive Protein and C-Reactive Protein-Based Scores to Predict Survival in Esophageal and Junctional Adenocarcinoma: Systematic Review and Meta-Analysis. Ann Surg Oncol 29, 1853–1865 (2022). https://doi.org/10.1245/s10434-021-10988-x

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  • DOI: https://doi.org/10.1245/s10434-021-10988-x

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