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Licensed Unlicensed Requires Authentication Published by De Gruyter May 12, 2023

Sex-specific disparities of serum pepsinogen I in relation to body mass index

  • Wenshen Xu , Bin Yang , Sheng Lin , Fuguo Zhan , Huijuan Chen , Xiaoming Qiu and Can Liu EMAIL logo

Abstract

Objectives

The clinical significance of serum pepsinogen (PG) for screening gastric cancer has been a controversial topic. Serum PG I levels have been demonstrated to be correlated with age, sex, and the Helicobacter pylori (HP) infection. However, the underlying factors that influence serum PG I variations remain to be fully elucidated. We aimed to evaluate the impacts of sex and body mass index (BMI) on PG I in Chinese population.

Methods

The cross-sectional study recruited 4,299 apparently healthy participants in Fujian Province. Serum PG levels were automatically measured using ELISA method. Serum H. pylori-IgG antibody was detected by the colloidal gold immunoassay. Clinical characteristics were obtained by questionnaire.

Results

Totally, 2,263 participants who had tests of serum PG and anti-HP IgG antibody were enrolled. Increased BMI and serum uric acid were observed in males with low PG I value (<70 μg/L). Multiple logistic regression showed the presence of overweight was the independent risk factor for male participants with low PG I level (odds ratio [OR] 1.519; p=0.017). However, the association was not found in females.

Conclusions

Sex-specific association of serum low PG I with overweight was observed in the southeast coastal areas of China. Thus, effects of sexual dimorphism should not be ignored during the clinical utilization of serum PG I.


Corresponding author: Can Liu, Department of Laboratory Medicine, the First Affiliated Hospital, Fujian Medical University, Fuzhou 350005, P.R. China; Department of Laboratory Medicine, National Regional Medical Center, Binhai Campus of the First Affiliated Hospital, Fujian Medical University, Fuzhou 350212, P.R. China; Fujian Key Laboratory of Laboratory Medicine, the First Affiliated Hospital, Fujian Medical University, Fuzhou, Fujian, P.R. China; Gene Diagnosis Research Center, Fujian Medical University, Fuzhou, P.R. China; Fujian Clinical Research Center for Clinical Immunology Laboratory Test, the First Affiliated Hospital, Fujian Medical University, Fuzhou, P.R. China; and 20 Chazhong Road, Fuzhou 350005, Fujian, P.R. China, Phone: +86 0591 87981971, Fax: +86 0591 87981029, E-mail:

Award Identifier / Grant number: grant number 82172327

  1. Research funding: This work was sponsored by National Natural Science Foundation of China [grant number 82172327].The funding organization played no role in the study design; in the collection, analysis, and interpretation of data; in the report; or in the decision to submit the report for publication.

  2. Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.

  3. Competing interests: The authors have no relevant financial or non-financial interests to disclose.

  4. Informed consent: Informed consent was obtained from all individuals included in this study.

  5. Ethical approval: The study was approved by the Ethics Committee of the First Affiliated Hospital of Fujian Medical University hospital in accordance with the Declaration of Helsinki.

References

1. Facts about overweight and obesity. http://www.who.int/mediacentre/factsheets/fs311/zh/index.html [Accessed June 2016].Search in Google Scholar

2. Pan, XF, Wang, L, Pan, A. Epidemiology and determinants of obesity in China. Lancet Diabetes Endocrinol 2021;9:373–92. https://doi.org/10.1016/s2213-8587(21)00045-0.Search in Google Scholar

3. Zheng, W, McLerran, DF, Rolland, B, Zhang, X, Inoue, M, Matsuo, K, et al.. Association between body-mass index and risk of death in more than 1 million Asians. N Engl J Med 2011;364:719–29. https://doi.org/10.1056/nejmoa1010679.Search in Google Scholar

4. Wu, Y, Li, Y, Giovannucci, E. Potential impact of time trend of lifestyle risk factors on burden of major gastrointestinal cancers in China. Gastroenterology 2021;161:1830–41.e8. https://doi.org/10.1053/j.gastro.2021.08.006.Search in Google Scholar PubMed

5. Lee, HW, Huang, D, Shin, WK, de la Torre, K, Yang, JJ, Song, M, et al.. Obesity at early adulthood increases risk of gastric cancer from the Health Examinees-Gem (HEXA-G) study. PLoS One 2022;17:e0260826. https://doi.org/10.1371/journal.pone.0260826.Search in Google Scholar PubMed PubMed Central

6. Larsson, SC, Burgess, S. Causal role of high body mass index in multiple chronic diseases: a systematic review and meta-analysis of Mendelian randomization studies. BMC Med 2021;19:320. https://doi.org/10.1186/s12916-021-02188-x.Search in Google Scholar PubMed PubMed Central

7. Loosen, SH, Roderburg, C, Jördens, MS, Fluegen, G, Luedde, T, Kostev, K. Overweight and obesity determine the risk for gastrointestinal cancer in a sex-dependent manner: a retrospective cohort study of 287,357 outpatients in Germany. Cancers (Basel) 2022;14:931. https://doi.org/10.3390/cancers14040931.Search in Google Scholar PubMed PubMed Central

8. Nam, SY, Jeong, J, Lee, WK, Jeon, SW. Sex-specific effect of body mass index and fasting glucose on gastric cancer risk and all causes mortality; a cohort study of 5.17 million. Int J Obes (Lond) 2022;46:1644–51. https://doi.org/10.1038/s41366-022-01161-9.Search in Google Scholar PubMed

9. Sung, H, Ferlay, J, Siegel, RL, Laversanne, M, Soerjomataram, I, Jemal, A, et al.. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA A Cancer J Clin 2021;71:209–49. https://doi.org/10.3322/caac.21660.Search in Google Scholar PubMed

10. Gastric Cancer Association, CACA. Consensus of Chinese expert panel on key difficult points of diagnosis and treatment in gastric cancer (2020 edition). Chin J Practical Surg 2020;8:869–904.Search in Google Scholar

11. Cai, Q, Zhu, C, Yuan, Y, Feng, Q, Feng, Y, Hao, Y, et al.. Development and validation of a prediction rule for estimating gastric cancer risk in the Chinese high-risk population: a nationwide multicentre study. Gut 2019;68:1576–87. https://doi.org/10.1136/gutjnl-2018-317556.Search in Google Scholar PubMed PubMed Central

12. Chapelle, N, Petryszyn, P, Blin, J, Leroy, M, Le Berre-Scoul, C, Jirka, I, et al.. A panel of stomach-specific biomarkers (GastroPanel®) for the diagnosis of atrophic gastritis: a prospective, multicenter study in a low gastric cancer incidence area. Helicobacter 2020;25:e12727. https://doi.org/10.1111/hel.12727.Search in Google Scholar PubMed

13. Chiang, TH, Chiu, SY, Chen, SL, Yen, AM, Fann, JC, Liu, CY, et al.. Serum pepsinogen as a predictor for gastric cancer death: a 16-year community-based cohort study. J Clin Gastroenterol 2019;53:e186–93. https://doi.org/10.1097/mcg.0000000000000992.Search in Google Scholar

14. 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.Search in Google Scholar PubMed

15. Sheng, C, Sun, L, Lyu, Z, Li, L, Zhang, Y, Zhang, Y, et al.. Development of a modified ABC method among Helicobacter pylori infected but serum pepsinogen test-negative individuals. Helicobacter 2023;28:e12966. https://doi.org/10.1111/hel.12966.Search in Google Scholar PubMed

16. Hu, Y, Bao, H, Jin, H, Zhao, J, Xu, Y, Huang, X, et al.. Performance evaluation of four prediction models for risk stratification in gastric cancer screening among a high-risk population in China. Gastric Cancer: Off J International Gastric Cancer Association Japanese Gastric Cancer Association 2021;24:1194–202. https://doi.org/10.1007/s10120-021-01204-6.Search in Google Scholar PubMed

17. Hatta, W, Koike, T, Asonuma, S, Okata, H, Uno, K, Oikawa, T, et al.. Smoking history and severe atrophic gastritis assessed by pepsinogen are risk factors for the prevalence of synchronous gastric cancers in patients with gastric endoscopic submucosal dissection: a multicenter prospective cohort study. J Gastroenterol 2023;58:433–43. https://doi.org/10.1007/s00535-023-01967-y.Search in Google Scholar PubMed

18. Hamashima, C. Update version of the Japanese guidelines for gastric cancer screening. Jpn J Clin Oncol 2018;48:673–83. https://doi.org/10.1093/jjco/hyy077.Search in Google Scholar PubMed

19. Kishino, T, Oyama, T, Tomori, A, Takahashi, A, Shinohara, T. Usefulness and limitations of a serum screening system to predict the risk of gastric cancer. Intern Med (Tokyo, Japan) 2020;59:1473–80. https://doi.org/10.2169/internalmedicine.3521-19.Search in Google Scholar PubMed PubMed Central

20. He, S, Sun, D, Li, H, Cao, M, Yu, X, Lei, L, et al.. Real-world practice of gastric cancer prevention and screening calls for practical prediction models. Clin Transl Gastroenterol 2023;14:e00546. https://doi.org/10.14309/ctg.0000000000000546.Search in Google Scholar PubMed PubMed Central

21. Fu, S, Hu, Q, Zhang, L, Li, Z. Effects of different pepsinogen cut offs in the screening of apparently healthy people. Clin Chem Lab Med 2022;60:e161–64. https://doi.org/10.1515/cclm-2022-0080.Search in Google Scholar PubMed

22. Kishikawa, H, Kimura, K, Ito, A, Arahata, K, Takarabe, S, Kaida, S, et al.. Cutoff pepsinogen level for predicting unintendedly eradicated cases of Helicobacter pylori infection in subjects with seemingly normal pepsinogen levels. Digestion 2017;95:229–36. https://doi.org/10.1159/000469705.Search in Google Scholar PubMed

23. Criteria of weight for adults. http://www.chinacdc.cn/jkzt/yyhspws/xzdc/201501/P020170721497677913633.pdf [Accessed 2013].Search in Google Scholar

24. Syrjänen, K, Eskelinen, M, Peetsalu, A, Sillakivi, T, Sipponen, P, Härkönen, M, et al.. GastroPanel® biomarker assay: the most comprehensive test for Helicobacter pylori infection and its clinical sequelae. A critical review. Anticancer Res 2019;39:1091–104. https://doi.org/10.21873/anticanres.13218.Search in Google Scholar PubMed

25. Syrjänen, K. Accuracy of serum biomarker panel (GastroPanel(®)) in the diagnosis of atrophic gastritis of the corpus. Systematic review and meta-analysis. Anticancer Res 2022;42:1679–96. https://doi.org/10.21873/anticanres.15645.Search in Google Scholar PubMed

26. Torisu, T, Matsumoto, T, Takata, Y, Ansai, T, Soh, I, Awano, S, et al.. Atrophic gastritis, but not antibody to Helicobacter pylori, is associated with body mass index in a Japanese population. J Gastroenterol 2008;43:762–6. https://doi.org/10.1007/s00535-008-2219-0.Search in Google Scholar PubMed

27. Cha, J, Jang, J. Clinical correlation between serum pepsinogen level and gastric atrophy in gastric neoplasm. Kor J Intern Med 2020;35:550–8. https://doi.org/10.3904/kjim.2018.282.Search in Google Scholar PubMed PubMed Central

28. Kutsuma, A, Oshida, H, Suwa, K, Nakajima, K. A possible association of low pepsinogen I and pepsinogen I/II with low and high body weight in Japanese men. Clin Biochem 2013;47:126–8. https://doi.org/10.1016/j.clinbiochem.2013.10.003.Search in Google Scholar PubMed

29. Razak, F, Anand, SS, Shannon, H, Vuksan, V, Davis, B, Jacobs, R, et al.. Defining obesity cut points in a multiethnic population. Circulation 2007;115:2111–8. https://doi.org/10.1161/circulationaha.106.635011.Search in Google Scholar

30. Castañeda, TR, Tong, J, Datta, R, Culler, M, Tschöp, MH. Ghrelin in the regulation of body weight and metabolism. Front Neuroendocrinol 2010;31:44–60. https://doi.org/10.1016/j.yfrne.2009.10.008.Search in Google Scholar PubMed

31. Eun Bae, S, Hoon Lee, J, Soo Park, Y, Ok Kim, S, Young Choi, J, Yong Ahn, J, et al.. Decrease of serum total ghrelin in extensive atrophic gastritis: comparison with pepsinogens in histological reference. Scand J Gastroenterol 2016;51:137–44. https://doi.org/10.3109/00365521.2015.1083049.Search in Google Scholar PubMed

32. Soriano-Guillen, L, Ortega, L, Navarro, P, Riestra, P, Gavela-Perez, T, Garces, C. Sex-related differences in the association of ghrelin levels with obesity in adolescents. Clin Chem Lab Med 2016;54:1371–6. https://doi.org/10.1515/cclm-2015-0555.Search in Google Scholar PubMed

33. Lin, XJ, Wang, CP, Liu, XD, Yan, KK, Li, S, Bao, HH, et al.. Body mass index and risk of gastric cancer: a meta-analysis. Jpn J Clin Oncol 2014;44:783–91. https://doi.org/10.1093/jjco/hyu082.Search in Google Scholar PubMed

34. Kim, HJ, Kim, N, Kim, HY, Lee, HS, Yoon, H, Shin, CM, et al.. Relationship between body mass index and the risk of early gastric cancer and dysplasia regardless of Helicobacter pylori infection. Gastric Cancer 2015;18:762–73. https://doi.org/10.1007/s10120-014-0429-0.Search in Google Scholar PubMed

35. McMenamin, ÚC, Liu, P, Kunzmann, AT, Cook, MB, Coleman, HG, Johnston, BT, et al.. Circulating sex hormones are associated with gastric and colorectal cancers but not esophageal adenocarcinoma in the UK biobank. Am J Gastroenterol 2021;116:522–9. https://doi.org/10.14309/ajg.0000000000001045.Search in Google Scholar PubMed PubMed Central

36. Camargo, MC, Goto, Y, Zabaleta, J, Morgan, DR, Correa, P, Rabkin, CS. Sex hormones, hormonal interventions, and gastric cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev 2012;21:20–38. https://doi.org/10.1158/1055-9965.epi-11-0834.Search in Google Scholar PubMed PubMed Central

37. Zhu, C, Cui, R, Gao, M, Rampersad, S, You, H, Sheng, C, et al.. The associations of serum uric acid with obesity-related acanthosis nigricans and related metabolic indices. Int J Endocrinol 2017;2017:5438157. https://doi.org/10.1155/2017/5438157.Search in Google Scholar PubMed PubMed Central

Received: 2023-03-05
Accepted: 2023-05-02
Published Online: 2023-05-12
Published in Print: 2023-10-26

© 2023 Walter de Gruyter GmbH, Berlin/Boston

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