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Remnant gastritis in gastric cancer patients causes loss of muscle mass 6 months after gastrectomy: a retrospective cohort study of Helicobacter pylori infection

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Abstract

Purpose

In this study, we assessed the relationship between remnant gastritis and muscle mass loss and then investigated the potential relationship between Helicobacter pylori (HP) infection and remnant gastritis and muscle loss.

Methods

We reviewed the medical records of 463 patients who underwent distal gastrectomy between January 2017 and March 2020. Of these patients, 100 with pStage I after laparoscopic surgery were included in this analysis.

Results

A multivariate analysis showed that the total Residue, Gastritis, Bile (RGB) classification score, which indicates the degree of gastritis, was significantly associated with the rate of change (rate of decrease) in the psoas muscle area (PMA) during the first 6 months after surgery (p = 0.014). Propensity score matching was performed according to HP infection, and the rate of change in the PMA and the degree of remnant gastritis in 56 patients were compared. Neither was significantly associated with HP infection.

Conclusions

Remnant gastritis did contribute to psoas muscle mass loss during the initial 6 months after gastrectomy, and HP infection was not significantly associated with either remnant gastritis or psoas muscle mass loss. Nevertheless, the potential for HP eradication to prevent muscle loss and improve the survival prognosis for gastrectomy patients merits further research.

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References

  1. Climent M, Munarriz M, Blazeby JM, Dorcaratto D, Ramón JM, Carrera MJ, et al. Weight loss and quality of life in patients surviving 2 years after gastric cancer resection. Eur J Surg Oncol. 2017;43:1337–413. https://doi.org/10.1016/j.ejso.2017.01.239.

    Article  PubMed  CAS  Google Scholar 

  2. Yu W, Seo BY, Chung HY. Postoperative body-weight loss and survival after curative resection for gastric cancer. Br J Surg. 2002;89:467–70. https://doi.org/10.1046/j.0007-1323.2001.02046.x.

    Article  PubMed  CAS  Google Scholar 

  3. Kuwada K, Kuroda S, Kikuchi S, Yoshida R, Nishizaki M, Kagawa S, et al. Clinical impact of sarcopenia on gastric cancer. Anticancer Res. 2019;39:2241–9. https://doi.org/10.21873/anticanres.13340.

    Article  PubMed  Google Scholar 

  4. Dodson S, Baracos VE, Jatoi A, Evans WJ, Cella D, Dalton JT, et al. Muscle wasting in cancer cachexia: clinical implications, diagnosis, and emerging treatment strategies. Annu Rev Med. 2011;62:265–79. https://doi.org/10.1146/annurev-med-061509-131248.

    Article  PubMed  CAS  Google Scholar 

  5. Mansoor O, Beaufrere B, Boirie Y, Ralliere C, Taillandier D, Aurousseau E, et al. Increased mRNA levels for components of the lysosomal, Ca2+-activated, and ATP-ubiquitin-dependent proteolytic pathways in skeletal muscle from head trauma patients. Proc Natl Acad Sci USA. 1996;93:2714–8. https://doi.org/10.1073/pnas.93.7.2714.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Adams JF. The clinical and metabolic consequences of total gastrectomy. I. Morbidity, weight, and nutrition. Scand J Gastroenterol. 1967;2:137–49. https://doi.org/10.3109/00365526709180059.

    Article  PubMed  CAS  Google Scholar 

  7. Yong HL, Seung JH, Hyeon CK, Woo JH, Joon SL, Kwangsuk L, et al. Gastrectomy for early gastric cancer is associated with decreased cardiovascular mortality in association with postsurgical metabolic changes. Ann Surg Oncol. 2013;20:1250–7. https://doi.org/10.1245/s10434-012-2688-5.

    Article  Google Scholar 

  8. Ji HP, Eunjung K, Eun MS, Seong HK, Do JP, Han KY, et al. Prediction model for screening patients at risk of malnutrition after gastric cancer surgery. Ann Surg Oncol. 2021;22:4471–81. https://doi.org/10.1245/s10434-020-09559-3.

    Article  Google Scholar 

  9. Fein M, Fuchs KH, Thalheimer A, Freys SM, Heimbucher J, Thiede A, et al. Long-term benefits of Roux-en-Y pouch reconstruction after total gastrectomy: a randomized trial. Ann Surg. 2008;247:759–65. https://doi.org/10.1097/SLA.0b013e318167748c.

    Article  PubMed  Google Scholar 

  10. Kurokawa Y. How can sarcopenia be prevented after gastrointestinal surgery? Ann Gastroenterol Surg. 2022;5(6):604–5. https://doi.org/10.1002/ags3.12617.

    Article  Google Scholar 

  11. Ritchie WP. Alkaline reflux gastritis: a critical reappraisal. Gut. 1984;25:975–87. https://doi.org/10.1136/gut.25.9.975.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Takiguchi S, Takata A, Murakami K, Miyazaki Y, Yanagimoto Y, Kurokawa Y, et al. Clinical application of ghrelin administration for gastric cancer patients undergoing gastrectomy. Gastric Cancer. 2014;17:200–5. https://doi.org/10.1007/s10120-013-0300-8.

    Article  PubMed  CAS  Google Scholar 

  13. Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K, et al. A role for ghrelin in the central regulation of feeding. Nature. 2001;409:194–8. https://doi.org/10.1038/35051587.

    Article  PubMed  CAS  Google Scholar 

  14. Fujitsuka N, Asakawa A, Amitani H, Fujimiya M, Inui A. Ghrelin and gastrointestinal movement. Methods Enzymol. 2012;514:289–301. https://doi.org/10.1016/B978-0-12-381272-8.00018-0.

    Article  PubMed  CAS  Google Scholar 

  15. Fujimiya M, Ataka K, Asakawa A, Chen CY, Kato I, Inui A. Ghrelin, des-acyl ghrelin and obestatin on the gastrointestinal motility. Peptides. 2011;32:2348–51. https://doi.org/10.1016/j.peptides.2011.07.020.

    Article  PubMed  CAS  Google Scholar 

  16. Falkén Y, Webb DL, Abraham-Nordling M, Kressner U, Hellström PM, Näslund E. Intravenous ghrelin accelerates postoperative gastric emptying and time to first bowel movement in humans. Neurogastroenterol Motil. 2013;25:474–80. https://doi.org/10.1111/nmo.12098.

    Article  PubMed  CAS  Google Scholar 

  17. Fujihata S, Sakuramoto S, Morimoto Y, Matsui K, Nishibeppu K, et al. Impact of loss of skeletal muscle mass within 6–12 months after gastrectomy and S1 adjuvant chemotherapy on the survival prognosis of elderly patients with gastric cancer. Surg Today. 2022;52:1472–83. https://doi.org/10.1007/s00595-022-02489-5.

    Article  PubMed  Google Scholar 

  18. Ikeda T, Kawano H, Hisamatsu Y, Ando K, Saeki H, et al. Progression from laparoscopic-assisted to totally laparoscopic distal gastrectomy: comparison of circular stapler (i-DST) and linear stapler (BBT) for intracorporeal anastomosis. Surg Endosc. 2013;27:325–32. https://doi.org/10.1007/s00464-012-2433-y.

    Article  PubMed  Google Scholar 

  19. Misawa K, Terashima M, Uenosono Y, Ota S, Hata H, et al. Evaluation of postgastrectomy symptoms after distal gastrectomy with Billroth-I reconstruction using the Postgastrectomy Syndrome Assessment Scale-45 (PGSAS-45). Gastric Cancer. 2015;18:675–81. https://doi.org/10.1007/s10120-014-0407-6.

    Article  PubMed  Google Scholar 

  20. Japanese Gastric Cancer Treatment Guidelines 2014 (ver. 4). Japanese Gastric Cancer Association. Gastric Cancer. 2017;20:1–19. https://doi.org/10.1007/s10120-016-0622-4.

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

    PubMed  CAS  Google Scholar 

  22. Kishikawa H, Kimura K, Takarabe S, Kaida S, Nishida J. Helicobacter pylori antibody titer and gastric cancer screening. Dis Mark. 2015;2015: 156719. https://doi.org/10.1155/2015/156719.

    Article  CAS  Google Scholar 

  23. Yamaji Y, Mitsushima T, Ikuma H, Okamoto M, Yoshida H, Kawabe T, et al. Weak response of helicobacter pylori antibody is high risk for gastric cancer: a cross-sectional study of 10,234 endoscoped Japanese. Scand J Gastroenterol. 2002;37:148–53. https://doi.org/10.1080/003655202753416795.

    Article  PubMed  CAS  Google Scholar 

  24. Tatemichi M, Sasazuki S, Inoue M, Tsugane S, JPHC Study Group. Clinical significance of IgG antibody titer against Helicobacter pylori. Helicobacter. 2009;14:231–6. https://doi.org/10.1111/j.1523-5378.2009.00681.x.

    Article  PubMed  CAS  Google Scholar 

  25. Kawai T, Itou K, Aoyama N, Murakami K, Kato K, The Japanese Society of Helicobacter Research, et al. Evaliation of gastric cancer risk by optimaized serum antibody titers against H. pylori: a multi-center retrospective studdy (in Japanese). Jpn J Helicobacter Res. 2020;22:51–7.

    Google Scholar 

  26. Kubo M, Sasako M, Gotoda T, Ono H, Fujishiro M, Saito D, et al. Endoscopic evaluation of the remnant stomach after gastrectomy: proposal for a new classification. Gastric Cancer. 2002;5:83–9. https://doi.org/10.1007/s101200200014.

    Article  PubMed  Google Scholar 

  27. Azuma T, Suto H, Ito Y, Muramatsu A, Ohtani M, Dojo M, et al. Eradication of Helicobacter pylori infection induces an increase in body mass index. Aliment Pharmacol Ther. 2002;16:240–4. https://doi.org/10.1046/j.1365-2036.16.s2.31.x.

    Article  PubMed  Google Scholar 

  28. Furuta T, Shirai N, Xiao F, Takashima M, Hanai H. Effect of Helicobacter pylori infection and its eradication on nutrition. Aliment Pharmacol Ther. 2002;16:799–806. https://doi.org/10.1046/j.1365-2036.2002.01222.x.

    Article  PubMed  CAS  Google Scholar 

  29. Patel P, Mendall MA, Khulusi S, Northfield TC, Strachan DP. Helicobacter pylori infection in childhood: risk factors and effect on growth. BMJ. 1994;309:1119–23. https://doi.org/10.1136/bmj.309.6962.1119.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Hsu PI, Lai KH, Tseng HH, Liu YC, Yen MY, Lin CK, et al. Correlation of serum immunoglobulin G Helicobacter pylori antibody titers with histologic and endoscopic findings in patients with dyspepsia. J Clin Gastroenterol. 1997;25:587–91. https://doi.org/10.1097/00004836-199712000-00007.

    Article  PubMed  CAS  Google Scholar 

  31. Kreuning J, Lindeman J, Biemond I, Lamers CB. Relation between IgG and IgA antibody titres against Helicobacter pylori in serum and severity of gastritis in asymptomatic subjects. J Clin Pathol. 1994;47:227–31. https://doi.org/10.1136/jcp.47.3.227.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Sim JG, Kim CJ, Seo JK. The value of Helicobacter pylori IgG antibody in estimating the severity of gastritis in children. J Korean Med Sci. 1995;10:329–33. https://doi.org/10.3346/jkms.1995.10.5.329.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Chen TS, Li FY, Chang FY, Lee SD. Immunoglobulin G antibody against Helicobacter pylori: clinical implications of levels found in serum. Clin Diagn Lab Immunol. 2002;9:1044–8. https://doi.org/10.1128/cdli.9.5.1044-1048.2002.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Yamamoto S, Yamasaki Y, Kuwata K, Yamasaki H, Nishida Y, Kobayashi Y. Role of Helicobacter pylori in residual gastritis after distal partial gastrectomy. World J Surg. 1998;22:28–34. https://doi.org/10.1007/s002689900345.

    Article  PubMed  CAS  Google Scholar 

  35. Lee Y, Tokunaga A, Tajiri T, Masuda G, Okuda T, Fujita I, et al. Inflammation of the gastric remnant after gastrectomy: mucosal erythema is associated with bile reflux and inflammatory cellular infiltration is associated with Helicobacter pylori infection. J Gastroenterol. 2004;39:520–6. https://doi.org/10.1007/s00535-003-1337-y.

    Article  PubMed  Google Scholar 

  36. Nagahata Y, Kawakita N, Azumi Y, Numata N, Yano M, Saitoh Y. Etiological involvement of Helicobacter pylori in “reflux” gastritis after gastrectomy. Am J Gastroenterol. 1996;91:2130–4.

    PubMed  CAS  Google Scholar 

  37. Isomoto H, Ueno H, Saenko VA, Mondal MS, Nishi Y, Kawano N, et al. Impact of Helicobacter pylori infection on gastric and plasma ghrelin dynamics in humans. Am J Gastroenterol. 2005;100:1711–20. https://doi.org/10.1111/j.1572-0241.2005.41492.x.

    Article  PubMed  CAS  Google Scholar 

  38. Isomoto H, Ueno H, Nishi Y, Yasutake T, Tanaka K, Kawano N, et al. Circulating ghrelin levels in patients with various upper gastrointestinal diseases. Dig Dis Sci. 2005;50:833–8. https://doi.org/10.1007/s10620-005-2648-z.

    Article  PubMed  CAS  Google Scholar 

  39. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa H. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature. 1999;402:656–60. https://doi.org/10.1038/45230.

    Article  PubMed  CAS  Google Scholar 

  40. Gonzalez-Rey E, Chorny A, Delgado M. Therapeutic action of ghrelin in a mouse model of colitis. Gastroenterology. 2006;130:1707–20. https://doi.org/10.1053/j.gastro.2006.01.041.

    Article  PubMed  CAS  Google Scholar 

  41. Aoyama T, Nakazono M, Nagasawa S, Segami K. Clinical impact of a perioperative exercise program for sarcopenia and overweight/obesity gastric cancer. In Vivo. 2021;35:707–12. https://doi.org/10.21873/invivo.12311.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Ida S, Kumagai K, Nunobe S. Current status of perioperative nutritional intervention and exercise in gastric cancer surgery: a review. Ann Gastroenterol Surg. 2021;6:197–203. https://doi.org/10.1002/ags3.12520.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Yamazaki R, Hatao F, Itokawa M, Morikawa Y, Honda M, Imamura K, et al. Impact of super energy-dense oral nutritional supplementation (SED ONS) on glycemic variability and food intake postoperatively in gastric cancer patients. Surg Today. 2022. https://doi.org/10.1007/s00595-022-02600-w. (Online ahead of print).

    Article  PubMed  Google Scholar 

  44. Malfertheiner P, Megraud F, O’Morain CA, Atherton J, Axon ATR, Bazzoli F, et al. Management of Helicobacter pylori infection—the Maastricht IV/Florence Consensus Report. Gut. 2012;61:646–64. https://doi.org/10.1136/gutjnl-2012-302084.

    Article  PubMed  CAS  Google Scholar 

  45. Fock KM, Talley N, Moayyedi P, Hunt R, Azuma T, Sugano K, et al. Asia-Pacific consensus guidelines on gastric cancer prevention. J Gastroenterol Hepatol. 2008;23:351–65. https://doi.org/10.1111/j.1440-1746.2008.05314.x.

    Article  PubMed  Google Scholar 

  46. Meimarakis G, Winter H, Assmann I, Kopp R, Lehn N, Kist M, et al. Helicobacter pylori as a prognostic indicator after curative resection of gastric carcinoma: a prospective study. Lancet Oncol. 2006;7:211–22. https://doi.org/10.1016/S1470-2045(06)70586-1.

    Article  PubMed  Google Scholar 

  47. Toftgaard C. Gastric cancer after peptic ulcer surgery: a historic prospective cohort investigation. Ann Surg. 1989;210:159–64. https://doi.org/10.1097/00000658-198908000-00004.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Fiore AC, Malangoni MA, Broadie TA, Madura JA, Jesseph IE. Surgical management of alkaline reflux gastritis. Arch Surg. 1982;117:689–94. https://doi.org/10.1001/archsurg.1982.01380290135024.

    Article  PubMed  CAS  Google Scholar 

  49. Dixon MF, Mapstone NP, Neville PM, Moayyedi P, Axon ATR. Bile reflux gastritis and intestinal metaplasia at the cardia. Gut. 2002;51:351–5. https://doi.org/10.1136/gut.51.3.351.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Santarelli L, Gabrielli M, Candelli M, Cremonini F, Nista EC, Cammarota G, et al. Post-cholecystectomy alkaline reactive gastritis: a randomized trial comparing sucralfate versus rabeprazole or no treatment. Eur J Gastroenterol Hepatol. 2003;15:975–9. https://doi.org/10.1097/00042737-200309000-00006.

    Article  PubMed  CAS  Google Scholar 

  51. Chen SL, Ji JR, Ping X, Cao ZJ, Mo JZ, Fang JY, et al. Effect of domperidone therapy on nocturnal dyspeptic symptoms of functional dyspepsia patients. World J Gastroenterol. 2010;16:613–7. https://doi.org/10.3748/wjg.v16.i5.613.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Osugi H, Fukuhara K, Takada N, Takemura M, Kinoshita H. Reconstructive procedure after distal gastrectomy to prevent remnant gastritis. Hepatogastroenterology. 2004;51:1215–8.

    PubMed  CAS  Google Scholar 

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Fujihata, S., Sakuramoto, S., Morimoto, Y. et al. Remnant gastritis in gastric cancer patients causes loss of muscle mass 6 months after gastrectomy: a retrospective cohort study of Helicobacter pylori infection. Surg Today 54, 152–161 (2024). https://doi.org/10.1007/s00595-023-02712-x

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