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Published in: BMC Gastroenterology 1/2017

Open Access 01-12-2017 | Research article

The potential value of serum pepsinogen for the diagnosis of atrophic gastritis among the health check-up populations in China: a diagnostic clinical research

Authors: Yuling Tong, Yulian Wu, Zhenya Song, Yingying Yu, Xinyan Yu

Published in: BMC Gastroenterology | Issue 1/2017

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Abstract

Background

The aim of this study is to assess the validity of the measurement of pepsinogen as a screening test for chronic atrophic gastritis (AG) in health check-up populations in China.

Methods

Patients from consecutive regular health check-up were enrolled from January 2014 to June 2015. Endoscopy, combined with monitoring the Helicobacter pylori (Hp) infections, and measuring the serum pepsinogen (PG) were used to determine the diagnostic accuracy of PG for the screening of atrophic gastritis. Histopathology was assessed by the Operative Link on Gastritis Assessment (OLGA) system. Statistical analysis was performed using SPSS statistical software.

Results

The total Hp infection rate was 40%. Based on pathology, the 996 participants were divided into three groups: non-atrophic (NAG), mild-moderate atrophic (MAG): stage I and II of the OLGA classification, and severe atrophic (SAG): stage III and IV of the OLGA classification. Compared with NAG and MAG groups, PGR decreased significantly in SAG group (p < 0.05). PGI and PGII levels were significantly elevated in Hp-positive group, while the PGR was markedly decreased (p < 0.01). When MAG and SAG groups were combined and compared with NAG group, the best cutoff value for atrophy diagnosis was PGI ≤50.3 ng/ml; the cutoff value in Hp-negative group was absolutely higher than in Hp-positive group. When NAG and MAG groups were combined and compared with the SAG group, the best cutoff value for diagnosis of severe atrophy was at PGR ≤4.28. The cutoff values in Hp-negative and Hp-positive groups were calculated at PGR ≤6.28 and ≤4.28, respectively.

Conclusions

Pepsinogens play an important role in the identification of patients with atrophic gastritis and severe AG. Use of different cutoff values of PG for Hp-negative and Hp-positive groups may offer greater efficacy in the diagnosis of AG.
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Literature
1.
go back to reference Cheli R, Simon L, Aste H, Figus IA, Nicolo G, Bajtai A, et al. Atrophic gastritis and intestinal metaplasia in asymptomatic Hungarian and Italian populations. Endoscopy. 1980;12:105–8.CrossRefPubMed Cheli R, Simon L, Aste H, Figus IA, Nicolo G, Bajtai A, et al. Atrophic gastritis and intestinal metaplasia in asymptomatic Hungarian and Italian populations. Endoscopy. 1980;12:105–8.CrossRefPubMed
2.
go back to reference Kato I, Tominaga S, Ito Y, Kobayashi S, Yoshii Y, Matsuura A, et al. Atrophic gastritis and stomach cancer risk: cross-sectional analyses. Jpn J Cancer Res. 1992;83:1041–6.CrossRefPubMed Kato I, Tominaga S, Ito Y, Kobayashi S, Yoshii Y, Matsuura A, et al. Atrophic gastritis and stomach cancer risk: cross-sectional analyses. Jpn J Cancer Res. 1992;83:1041–6.CrossRefPubMed
3.
go back to reference Kato I, Tominaga S, Ito Y, Kobayashi S, Yoshii Y, Matsuura A, et al. A prospective study of atrophic gastritis and stomach cancer risk. Jpn J Cancer Res. 1992;83:1137–42.CrossRefPubMed Kato I, Tominaga S, Ito Y, Kobayashi S, Yoshii Y, Matsuura A, et al. A prospective study of atrophic gastritis and stomach cancer risk. Jpn J Cancer Res. 1992;83:1137–42.CrossRefPubMed
4.
go back to reference Namekata T, Miki K, Kimmey M, Fritsche T, Hughes D, Moore D, et al. Chronic atrophic gastritis and Helicobacter pylori infection among Japanese Americans in Seattle. Am J Epidemiol. 2000;151:820–30.CrossRefPubMed Namekata T, Miki K, Kimmey M, Fritsche T, Hughes D, Moore D, et al. Chronic atrophic gastritis and Helicobacter pylori infection among Japanese Americans in Seattle. Am J Epidemiol. 2000;151:820–30.CrossRefPubMed
5.
go back to reference de Vries AC, van Grieken NC, Looman CW, Casparie MK, de Vries E, Meijer GA, et al. Gastric cancer risk in patients with premalignant gastric lesions: a nationwide cohort study in the Netherlands. Gastroenterology. 2008;134:945–52.CrossRefPubMed de Vries AC, van Grieken NC, Looman CW, Casparie MK, de Vries E, Meijer GA, et al. Gastric cancer risk in patients with premalignant gastric lesions: a nationwide cohort study in the Netherlands. Gastroenterology. 2008;134:945–52.CrossRefPubMed
6.
7.
go back to reference Rugge M, Correa P, Di Mario F, El-Omar E, Fiocca R, Geboes K, et al. OLGA staging for gastritis: a tutorial. Dig Liver Dis. 2008;40:650–8.CrossRefPubMed Rugge M, Correa P, Di Mario F, El-Omar E, Fiocca R, Geboes K, et al. OLGA staging for gastritis: a tutorial. Dig Liver Dis. 2008;40:650–8.CrossRefPubMed
8.
go back to reference Rugge M, de Boni M, Pennelli G, de Bona M, Giacomelli L, Fassan M, et al. Gastritis OLGA-staging and gastric cancer risk: a twelve-year clinico-pathological follow-up study. Aliment Pharmacol Ther. 2010;31:1104–11.PubMed Rugge M, de Boni M, Pennelli G, de Bona M, Giacomelli L, Fassan M, et al. Gastritis OLGA-staging and gastric cancer risk: a twelve-year clinico-pathological follow-up study. Aliment Pharmacol Ther. 2010;31:1104–11.PubMed
9.
go back to reference Quach DT, Le HM, Nguyen OT, Nguyen TS, Uemura N. The severity of endoscopic gastric atrophy could help to predict Operative Link on gastritis assessment gastritis stage. J Gastroenterol Hepatol. 2011;26:281–5.CrossRefPubMed Quach DT, Le HM, Nguyen OT, Nguyen TS, Uemura N. The severity of endoscopic gastric atrophy could help to predict Operative Link on gastritis assessment gastritis stage. J Gastroenterol Hepatol. 2011;26:281–5.CrossRefPubMed
10.
go back to reference Pasechnikov V, Chukov S, Fedorov E, Kikuste I, Leja M. Gastric cancer: prevention, screening and early diagnosis. World J Gastroenterol. 2014;20:13842–62.CrossRefPubMedPubMedCentral Pasechnikov V, Chukov S, Fedorov E, Kikuste I, Leja M. Gastric cancer: prevention, screening and early diagnosis. World J Gastroenterol. 2014;20:13842–62.CrossRefPubMedPubMedCentral
11.
go back to reference Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney system. International workshop on the histopathology of gastritis, Houston 1994. Am J Surg Pathol. 1996;20:1161–81.CrossRefPubMed Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney system. International workshop on the histopathology of gastritis, Houston 1994. Am J Surg Pathol. 1996;20:1161–81.CrossRefPubMed
12.
go back to reference Shikata K, Ninomiya T, Yonemoto K, Ikeda F, Hata J, Doi Y, et al. Optimal cutoff value of the serum pepsinogen level for prediction of gastric cancer incidence: the Hisayama study. Scand J Gastroenterol. 2012;47:669–75.CrossRefPubMed Shikata K, Ninomiya T, Yonemoto K, Ikeda F, Hata J, Doi Y, et al. Optimal cutoff value of the serum pepsinogen level for prediction of gastric cancer incidence: the Hisayama study. Scand J Gastroenterol. 2012;47:669–75.CrossRefPubMed
14.
go back to reference Miki K. Gastric cancer screening by combined assay for serum anti-Helicobacter pylori IgG antibody and serum pepsinogen levels - "ABC method". Proc Jpn Acad Ser B Phys Biol Sci. 2011;87:405–14.CrossRefPubMedPubMedCentral Miki K. Gastric cancer screening by combined assay for serum anti-Helicobacter pylori IgG antibody and serum pepsinogen levels - "ABC method". Proc Jpn Acad Ser B Phys Biol Sci. 2011;87:405–14.CrossRefPubMedPubMedCentral
15.
go back to reference Watabe H, Mitsushima T, Yamaji Y, Okamoto M, Wada R, Kokubo T, et al. Predicting the development of gastric cancer from combining Helicobacter pylori antibodies and serum pepsinogen status: a prospective endoscopic cohort study. Gut. 2005;54:764–8.CrossRefPubMedPubMedCentral Watabe H, Mitsushima T, Yamaji Y, Okamoto M, Wada R, Kokubo T, et al. Predicting the development of gastric cancer from combining Helicobacter pylori antibodies and serum pepsinogen status: a prospective endoscopic cohort study. Gut. 2005;54:764–8.CrossRefPubMedPubMedCentral
16.
go back to reference Inoue K, Fujisawa T, Haruma K. Assessment of degree of health of the stomach by concomitant measurement of serum pepsinogen and serum Helicobacter pylori antibodies. Int J Biol Markers. 2010;25:207–12.PubMed Inoue K, Fujisawa T, Haruma K. Assessment of degree of health of the stomach by concomitant measurement of serum pepsinogen and serum Helicobacter pylori antibodies. Int J Biol Markers. 2010;25:207–12.PubMed
17.
go back to reference Nasrollahzadeh D, Aghcheli K, Sotoudeh M, Shakeri R, Persson EC, Islami F, et al. Accuracy and cut-off values of pepsinogens I, II and gastrin 17 for diagnosis of gastric fundic atrophy: influence of gastritis. PLoS One. 2011;6:e26957.CrossRefPubMedPubMedCentral Nasrollahzadeh D, Aghcheli K, Sotoudeh M, Shakeri R, Persson EC, Islami F, et al. Accuracy and cut-off values of pepsinogens I, II and gastrin 17 for diagnosis of gastric fundic atrophy: influence of gastritis. PLoS One. 2011;6:e26957.CrossRefPubMedPubMedCentral
18.
19.
go back to reference Graham DY, Nurgalieva ZZ, El-Zimaity HM, Opekun AR, Campos A, Guerrero L, et al. Noninvasive versus histologic detection of gastric atrophy in a Hispanic population in North America. Clin Gastroenterol Hepatol. 2006;4:306–14.CrossRefPubMed Graham DY, Nurgalieva ZZ, El-Zimaity HM, Opekun AR, Campos A, Guerrero L, et al. Noninvasive versus histologic detection of gastric atrophy in a Hispanic population in North America. Clin Gastroenterol Hepatol. 2006;4:306–14.CrossRefPubMed
20.
go back to reference Bornschein J, Selgrad M, Wex T, Kuester D, Malfertheiner P. Serological assessment of gastric mucosal atrophy in gastric cancer. BMC Gastroenterol. 2012;12:10.CrossRefPubMedPubMedCentral Bornschein J, Selgrad M, Wex T, Kuester D, Malfertheiner P. Serological assessment of gastric mucosal atrophy in gastric cancer. BMC Gastroenterol. 2012;12:10.CrossRefPubMedPubMedCentral
21.
go back to reference Lomba-Viana R, Dinis-Ribeiro M, Fonseca F, Vieira AS, Bento MJ, Lomba-Viana H. Serum pepsinogen test for early detection of gastric cancer in a European country. Eur J Gastroenterol Hepatol. 2012;24:37–41.CrossRefPubMed Lomba-Viana R, Dinis-Ribeiro M, Fonseca F, Vieira AS, Bento MJ, Lomba-Viana H. Serum pepsinogen test for early detection of gastric cancer in a European country. Eur J Gastroenterol Hepatol. 2012;24:37–41.CrossRefPubMed
22.
go back to reference Leja M, Kupcinskas L, Funka K, Sudraba A, Jonaitis L, Ivanauskas A, et al. The validity of a biomarker method for indirect detection of gastric mucosal atrophy versus standard histopathology. Dig Dis Sci. 2009;54:2377–84.CrossRefPubMed Leja M, Kupcinskas L, Funka K, Sudraba A, Jonaitis L, Ivanauskas A, et al. The validity of a biomarker method for indirect detection of gastric mucosal atrophy versus standard histopathology. Dig Dis Sci. 2009;54:2377–84.CrossRefPubMed
23.
go back to reference Kikuchi S, Kato M, Katsuyama T, Tominaga S, Asaka M. Design and planned analyses of an ongoing randomized trial assessing the preventive effect of Helicobacter pylori eradication on occurrence of new gastric carcinomas after endoscopic resection. Helicobacter. 2006;11:147–51.CrossRefPubMed Kikuchi S, Kato M, Katsuyama T, Tominaga S, Asaka M. Design and planned analyses of an ongoing randomized trial assessing the preventive effect of Helicobacter pylori eradication on occurrence of new gastric carcinomas after endoscopic resection. Helicobacter. 2006;11:147–51.CrossRefPubMed
24.
go back to reference Kang JM, Kim N, Yoo JY, Park YS, Lee DH, Kim HY, et al. The role of serum pepsinogen and gastrin test for the detection of gastric cancer in Korea. Helicobacter. 2008;13:146–56.CrossRefPubMed Kang JM, Kim N, Yoo JY, Park YS, Lee DH, Kim HY, et al. The role of serum pepsinogen and gastrin test for the detection of gastric cancer in Korea. Helicobacter. 2008;13:146–56.CrossRefPubMed
25.
go back to reference Huang YK, Yu JC, Kang WM, Ma ZQ, Ye X, Tian SB, et al. Significance of serum pepsinogens as a biomarker for gastric cancer and atrophic gastritis screening: a systematic review and meta-analysis. PLoS One. 2015;10:e0142080.CrossRefPubMedPubMedCentral Huang YK, Yu JC, Kang WM, Ma ZQ, Ye X, Tian SB, et al. Significance of serum pepsinogens as a biomarker for gastric cancer and atrophic gastritis screening: a systematic review and meta-analysis. PLoS One. 2015;10:e0142080.CrossRefPubMedPubMedCentral
26.
go back to reference Cao Q, Ran ZH, Xiao SD. Screening of atrophic gastritis and gastric cancer by serum pepsinogen, gastrin-17 and Helicobacter pylori immunoglobulin G antibodies. J Dig Dis. 2007;8:15–22.CrossRefPubMed Cao Q, Ran ZH, Xiao SD. Screening of atrophic gastritis and gastric cancer by serum pepsinogen, gastrin-17 and Helicobacter pylori immunoglobulin G antibodies. J Dig Dis. 2007;8:15–22.CrossRefPubMed
27.
go back to reference Agreus L, Storskrubb T, Aro P, Ronkainen J, Talley NJ, Sipponen P. Clinical use of proton-pump inhibitors but not H2-blockers or antacid/alginates raises the serum levels of amidated gastrin-17, pepsinogen I and pepsinogen II in a random adult population. Scand J Gastroenterol. 2009;44:564–70.CrossRefPubMed Agreus L, Storskrubb T, Aro P, Ronkainen J, Talley NJ, Sipponen P. Clinical use of proton-pump inhibitors but not H2-blockers or antacid/alginates raises the serum levels of amidated gastrin-17, pepsinogen I and pepsinogen II in a random adult population. Scand J Gastroenterol. 2009;44:564–70.CrossRefPubMed
28.
go back to reference Asaka M, Kimura T, Kudo M, Takeda H, Mitani S, Miyazaki T, et al. Relationship of Helicobacter pylori to serum pepsinogens in an asymptomatic Japanese population. Gastroenterology. 1992;102:760–6.CrossRefPubMed Asaka M, Kimura T, Kudo M, Takeda H, Mitani S, Miyazaki T, et al. Relationship of Helicobacter pylori to serum pepsinogens in an asymptomatic Japanese population. Gastroenterology. 1992;102:760–6.CrossRefPubMed
29.
go back to reference Kiyohira K, Yoshihara M, Ito M, Haruma K, Tanaka S, Chayama K. Serum pepsinogen concentration as a marker of Helicobacter pyloriinfection and the histologic grade of gastritis; evaluation of gastric mucosa by serum pepsinogen levels. J Gastroenterol. 2003;38:332–8.CrossRefPubMed Kiyohira K, Yoshihara M, Ito M, Haruma K, Tanaka S, Chayama K. Serum pepsinogen concentration as a marker of Helicobacter pyloriinfection and the histologic grade of gastritis; evaluation of gastric mucosa by serum pepsinogen levels. J Gastroenterol. 2003;38:332–8.CrossRefPubMed
30.
go back to reference Nagy P, Johansson S, Molloy-Bland M. Systematic review of time trends in the prevalence of Helicobacter pylori infection in China and the USA. Gut Pathog. 2016;8:8.CrossRefPubMedPubMedCentral Nagy P, Johansson S, Molloy-Bland M. Systematic review of time trends in the prevalence of Helicobacter pylori infection in China and the USA. Gut Pathog. 2016;8:8.CrossRefPubMedPubMedCentral
31.
go back to reference Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345:784–9.CrossRefPubMed Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345:784–9.CrossRefPubMed
32.
go back to reference Roman LD, Lukyanchuk R, Sablin OA, Araslanova EI, Eklund C, Hendolin P, et al. Prevalence of H. Pylori infection and atrophic gastritis in a population-based screening with serum biomarker panel (GastroPanel(R)) in St. Petersburg. Anticancer Res. 2016;36:4129–38.PubMed Roman LD, Lukyanchuk R, Sablin OA, Araslanova EI, Eklund C, Hendolin P, et al. Prevalence of H. Pylori infection and atrophic gastritis in a population-based screening with serum biomarker panel (GastroPanel(R)) in St. Petersburg. Anticancer Res. 2016;36:4129–38.PubMed
33.
go back to reference Rugge M, Capelle LG, Cappellesso R, Nitti D, Kuipers EJ. Precancerous lesions in the stomach: from biology to clinical patient management. Best Pract Res Clin Gastroenterol. 2013;27:205–23.CrossRefPubMed Rugge M, Capelle LG, Cappellesso R, Nitti D, Kuipers EJ. Precancerous lesions in the stomach: from biology to clinical patient management. Best Pract Res Clin Gastroenterol. 2013;27:205–23.CrossRefPubMed
34.
go back to reference Samloff IM. Pepsinogens I and II: purification from gastric mucosa and radioimmunoassay in serum. Gastroenterology. 1982;82:26–33.PubMed Samloff IM. Pepsinogens I and II: purification from gastric mucosa and radioimmunoassay in serum. Gastroenterology. 1982;82:26–33.PubMed
35.
go back to reference Gritti I, Banfi G, Roi GS. Pepsinogens: physiology, pharmacology pathophysiology and exercise. Pharmacol Res. 2000;41:265–81.CrossRefPubMed Gritti I, Banfi G, Roi GS. Pepsinogens: physiology, pharmacology pathophysiology and exercise. Pharmacol Res. 2000;41:265–81.CrossRefPubMed
36.
go back to reference He CY, Sun LP, Gong YH, Xu Q, Dong NN, Yuan Y. Serum pepsinogen II: a neglected but useful biomarker to differentiate between diseased and normal stomachs. J Gastroenterol Hepatol. 2011;26:1039–46.CrossRefPubMed He CY, Sun LP, Gong YH, Xu Q, Dong NN, Yuan Y. Serum pepsinogen II: a neglected but useful biomarker to differentiate between diseased and normal stomachs. J Gastroenterol Hepatol. 2011;26:1039–46.CrossRefPubMed
37.
go back to reference Chae H, Lee JH, Lim J, Kim M, Kim Y, Han K, et al. Clinical utility of serum pepsinogen levels as a screening test of atrophic gastritis. Korean J Lab Med. 2008;28:201–6.CrossRefPubMed Chae H, Lee JH, Lim J, Kim M, Kim Y, Han K, et al. Clinical utility of serum pepsinogen levels as a screening test of atrophic gastritis. Korean J Lab Med. 2008;28:201–6.CrossRefPubMed
38.
go back to reference Zoalfaghari A, Aletaha N, Roushan N, Taslimi R, Foroutan H, Faridnia B. Accuracy of pepsinogens for early diagnosis of atrophic gastritis and gastric cancer in Iranian population. Med J Islam Repub Iran. 2014;28:150.PubMedPubMedCentral Zoalfaghari A, Aletaha N, Roushan N, Taslimi R, Foroutan H, Faridnia B. Accuracy of pepsinogens for early diagnosis of atrophic gastritis and gastric cancer in Iranian population. Med J Islam Repub Iran. 2014;28:150.PubMedPubMedCentral
39.
go back to reference Benberin V, Bektayeva R, Karabayeva R, Lebedev A, Akemeyeva K, Paloheimo L, et al. Prevalence of H. Pylori infection and atrophic gastritis among symptomatic and dyspeptic adults in Kazakhstan. A hospital-based screening study using a panel of serum biomarkers. Anticancer Res. 2013;33:4595–602.PubMed Benberin V, Bektayeva R, Karabayeva R, Lebedev A, Akemeyeva K, Paloheimo L, et al. Prevalence of H. Pylori infection and atrophic gastritis among symptomatic and dyspeptic adults in Kazakhstan. A hospital-based screening study using a panel of serum biomarkers. Anticancer Res. 2013;33:4595–602.PubMed
40.
go back to reference Telaranta-Keerie A, Kara R, Paloheimo L, Harkonen M, Sipponen P. Prevalence of undiagnosed advanced atrophic corpus gastritis in Finland: an observational study among 4,256 volunteers without specific complaints. Scand J Gastroenterol. 2010;45:1036–41.CrossRefPubMed Telaranta-Keerie A, Kara R, Paloheimo L, Harkonen M, Sipponen P. Prevalence of undiagnosed advanced atrophic corpus gastritis in Finland: an observational study among 4,256 volunteers without specific complaints. Scand J Gastroenterol. 2010;45:1036–41.CrossRefPubMed
41.
go back to reference Storskrubb T, Aro P, Ronkainen J, Sipponen P, Nyhlin H, Talley NJ, et al. Serum biomarkers provide an accurate method for diagnosis of atrophic gastritis in a general population: the Kalixanda study. Scand J Gastroenterol. 2008;43:1448–55.CrossRefPubMed Storskrubb T, Aro P, Ronkainen J, Sipponen P, Nyhlin H, Talley NJ, et al. Serum biomarkers provide an accurate method for diagnosis of atrophic gastritis in a general population: the Kalixanda study. Scand J Gastroenterol. 2008;43:1448–55.CrossRefPubMed
42.
go back to reference Zhou L, Lin S, Ding S, Huang X, Jin Z, Cui R, et al. Relationship of Helicobacter pylori eradication with gastric cancer and gastric mucosal histological changes: a 10-year follow-up study. Chin Med J (Engl). 2014;127:1454–8. Zhou L, Lin S, Ding S, Huang X, Jin Z, Cui R, et al. Relationship of Helicobacter pylori eradication with gastric cancer and gastric mucosal histological changes: a 10-year follow-up study. Chin Med J (Engl). 2014;127:1454–8.
43.
go back to reference Valle J, Kekki M, Sipponen P, Ihamaki T, Siurala M. Long-term course and consequences of Helicobacter pylori gastritis. Results of a 32-year follow-up study. Scand J Gastroenterol. 1996;31:546–50.CrossRefPubMed Valle J, Kekki M, Sipponen P, Ihamaki T, Siurala M. Long-term course and consequences of Helicobacter pylori gastritis. Results of a 32-year follow-up study. Scand J Gastroenterol. 1996;31:546–50.CrossRefPubMed
44.
go back to reference Villako K, Kekki M, Maaroos HI, Sipponen P, Uibo R, Tammur R, et al. Chronic gastritis: progression of inflammation and atrophy in a six-year endoscopic follow-up of a random sample of 142 Estonian urban subjects. Scand J Gastroenterol Suppl. 1991;186:135–41.CrossRefPubMed Villako K, Kekki M, Maaroos HI, Sipponen P, Uibo R, Tammur R, et al. Chronic gastritis: progression of inflammation and atrophy in a six-year endoscopic follow-up of a random sample of 142 Estonian urban subjects. Scand J Gastroenterol Suppl. 1991;186:135–41.CrossRefPubMed
45.
go back to reference Kekki M, Ihamaki T, Saukkonen M, Varis K, Siurala M. Progression of gastritis at a population level. Comparison of a long-term follow-up with stochastic analysis of cross-sectional data. Scand J Gastroenterol. 1980;15:651–5.CrossRefPubMed Kekki M, Ihamaki T, Saukkonen M, Varis K, Siurala M. Progression of gastritis at a population level. Comparison of a long-term follow-up with stochastic analysis of cross-sectional data. Scand J Gastroenterol. 1980;15:651–5.CrossRefPubMed
46.
go back to reference Haj-Sheykholeslami A, Rakhshani N, Amirzargar A, Rafiee R, Shahidi SM, Nikbin B, et al. Serum pepsinogen I, pepsinogen II, and gastrin 17 in relatives of gastric cancer patients: comparative study with type and severity of gastritis. Clin Gastroenterol Hepatol. 2008;6:174–9.CrossRefPubMed Haj-Sheykholeslami A, Rakhshani N, Amirzargar A, Rafiee R, Shahidi SM, Nikbin B, et al. Serum pepsinogen I, pepsinogen II, and gastrin 17 in relatives of gastric cancer patients: comparative study with type and severity of gastritis. Clin Gastroenterol Hepatol. 2008;6:174–9.CrossRefPubMed
Metadata
Title
The potential value of serum pepsinogen for the diagnosis of atrophic gastritis among the health check-up populations in China: a diagnostic clinical research
Authors
Yuling Tong
Yulian Wu
Zhenya Song
Yingying Yu
Xinyan Yu
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Gastroenterology / Issue 1/2017
Electronic ISSN: 1471-230X
DOI
https://doi.org/10.1186/s12876-017-0641-6

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