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Cancer Epidemiology Biomarkers & Prevention Vol. 15, 1083-1094, June 2006
© 2006 American Association for Cancer Research

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Prevalence of Chronic Atrophic Gastritis in Different Parts of the World

Melanie Nicole Weck and Hermann Brenner

Division of Clinical Epidemiology and Aging Research, German Cancer Research Center, Heidelberg, Germany

Requests for reprints: Hermann Brenner, Division of Clinical Epidemiology and Aging Research, German Cancer Research Center, Bergheimer Straße 20, D-69115 Heidelberg, Germany. Phone: 49-6221-548140; Fax: 49-6221-548142. E-mail: h.brenner{at}dkfz-heidelberg.de


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Appendix 1
 References
 
Chronic atrophic gastritis (CAG) is a well-established precursor of intestinal gastric cancer, but epidemiologic data about its occurrence are sparse. We provide an overview on studies that examined the prevalence of CAG in different parts of the world. Articles containing data about the prevalence of chronic atrophic gastritis in unselected population samples and published until November 2005 were identified by searching the MEDLINE database. Furthermore, the references in the identified publications were screened for additional suitable studies. Studies comprising at least 50 subjects were included. Forty-one studies providing data on the prevalence of CAG in unselected population samples could be identified. CAG was determined by gastroscopy in 15 studies and by pepsinogen serum levels in 26 studies. Although results are difficult to compare due to the various definitions of CAG used, a strong increase with age, the lack of major gender differences, and strong variations between populations and population groups (in particular, relatively high rates in certain Asian populations) could be observed quite consistently. We conclude that CAG is relatively common among older adults in different parts of the world, but large variations exist. Large-scale international comparative studies with standardized methodology to determine CAG are needed to provide a coherent picture of the epidemiology of CAG in various populations. Noninvasive measurements of CAG by pepsinogen levels may be particularly suited for that purpose. (Cancer Epidemiol Biomarkers Prev 2006;15(6):1083–94)


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Appendix 1
 References
 
Chronic atrophic gastritis (CAG) plays a crucial role in the development of intestinal gastric cancer, the most common type of gastric cancer, which continues to be one of the leading cancer causes of death in the world. Mortality rates of gastric cancer are particularly high in Asia, South America, and parts of Europe (1). It is well established that gastric carcinogenesis is a continuous process leading from nonatrophic gastritis to glandular atrophy (loss of specialized glands), to metaplasia and dysplasia, and finally to adenocarcinoma (2, 3). This process usually takes decades and seems to be initiated by infection with the gastric bacterium Helicobacter pylori in many if not most cases (4-7). The long-term development may thus potentially provide opportunities for early detection of precancerous lesions and intervention. However, because the majority of individuals carrying CAG do not suffer from any symptoms, CAG and early-stage gastric cancer remain unrecognized in most cases.

Presence of CAG may be determined either by gastroscopy with subsequent histologic analysis of obtained biopsies (8) or by investigating the pepsinogen (PG I and PG II) concentrations in serum (9, 10); both PG I and the PG I/PG II ratio are decreased in CAG. A number of epidemiologic studies have meanwhile assessed the prevalence of CAG in different populations, but the selection of study samples and the definitions of CAG have been quite diverse. In this article, we provide a comprehensive review of published data on the prevalence of chronic atrophic gastritis, with particular attention to differences and similarities in the methods used. We thereby aim to delineate the current state of knowledge regarding the epidemiology of CAG and the need for further investigation.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Appendix 1
 References
 
Studies investigating the prevalence of chronic atrophic gastritis were identified by searching for articles in the MEDLINE database, using various combinations of the terms "chronic atrophic gastritis," "CAG," "prevalence," "atrophic gastritis," "atrophic," "gastritis," "(gastric) atrophy," "pespinogen(s)," "precancerous lesion(s)," "stomach", and "(mass) screening." The references in the thus acquired articles were also screened for suitable studies (cross-referencing). The analysis was restricted to studies published in English until November 30, 2005.

To ensure reasonable levels of precision of prevalence estimates, we excluded studies with <50 participants. We also excluded studies where patients were preselected according to gastrointestinal symptoms (e.g., gastroscopy-based studies where gastroscopy was employed due to symptoms rather than as a primary screening tool). These criteria were employed to avoid biased estimates of prevalences.

Information retrieved from the publications are place and time of the study, constitution of the study population, number of participants, male/female ratio, age (range and mean), type of measurement of CAG, and criteria for diagnosis. Whenever possible, the prevalence of CAG was extracted in terms of an overall value and stratified by gender, by age, and by location of the lesion (latter for gastroscopy screenings only). In some of the publications, the actual numbers were not stated but could be derived from published graphs.

According to type of measurement of CAG, the studies were grouped into gastroscopy-based screenings with subsequent histologic examination on one hand and in studies that determined serum pepsinogen levels on the other hand. Prevalences extracted from the gastroscopy-based studies include both CAG with and without more advanced lesions.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Appendix 1
 References
 
The literature search identified 89 studies providing data about CAG prevalences. Of these, 48 studies were excluded from this review for the following reasons: preselection of study population due to symptoms (44 studies) and size of the study population (four studies). References of excluded studies are given in Appendix 1.

As the numbers indicate, the selection of the study participants turns out to be the most critical criterion. It was paid close attention to exclude all studies showing any evidence of a preselection of participants related to gastritis. Nevertheless, not all included studies do include perfectly representative population samples. Study samples also accepted were blood donors, elderly people, hospital workers, industry workers, smokers, and people taking part in an annual health examination or a CVD screening and self-defense forces. These primarily non–population-based study populations were tolerated because even a selection via population registers cannot assure perfect random samples when taking response rates into account.

Among the 41 studies that met the inclusion criteria, there are 15 gastroscopy-based studies (11-28) and 26 studies measuring pepsinogen concentrations (29-60). In all but two of the latter, pepsinogen levels were measured by RIA; in the studies by Sipponen et al. (54) and Green et al. (59), measurements were done by enzyme immunoassay. Not all of the studies had the primary intention to determine the CAG prevalence. Some of the studies collected the data primarily for other purposes, such as to study the role of CAG and other risk factors in the development of gastric cancer (15, 18, 19, 32, 33, 35, 37, 43, 55, 56), or to assess the association of CAG with H. pylori infection (25, 44). An overview on the studies is given in Table 1 (gastroscopy-based studies) and Table 2 (studies based on serum pepsinogen levels), respectively.


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  		Table 1. Gastroscopy-based studies

 

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  		Table 2. Pepsinogen-based studies

 
Due to use of different methods of measurements and varying definitions and cut points, a direct comparison of prevalences among the studies is difficult. Despite this difficulty, a number of patterns become apparent when looking at the data.

Gastroscopy-based studies have been conducted in all continents except for Africa, with a main focus on high-risk areas of gastric cancer. In detail, they were done in Asia [Japan (25) and China (22, 26)], in Europe [Finland (11, 14), Estonia (12, 16), the Netherlands (13), Norway (20), Sweden (27), Italy (15, 18), and Hungary (15)], in Columbia (19), in Iran (28), and in Australia (24), with the first study being published in 1968 by Siurala et al. (11) from Finland. The number of participants varied widely among the different studies. By inclusion criteria, the smallest study population enclosed 50 participants. Most of the gastroscopy-based studies comprised between 100 and 250 participants, but there were also three studies examining >1,000 persons, the maximum number being 3,400. One study was restricted to males, all others comprised both males and females. The age of participants varied considerably among the studies because some population registry-based studies investigated people with an age range from 16 to 69 years, but narrower age ranges were included in several other studies.

Prevalence rates vary widely between the populations screened by gastroscopy and even within population groups. Although most studies show prevalences below 50%, some studies conducted in Japan and China reveal much higher prevalences (22, 25, 26). An increase of CAG prevalence with age was consistently found in most studies looking at age-specific prevalences. However, two studies (22, 26) from a Chinese population with one of the world's highest rates of stomach cancer showed prevalences of CAG or even more advanced lesions close to 100% even among the youngest of the included age groups. Most studies do not reveal any differences between males and females. Except for one study (16), CAG was always more frequent in the antrum than in the fundus/corpus.

Measurement of pepsinogen serum levels was carried out by 11 studies in Japan (33, 35, 44, 49, 51-53, 55-58), two studies among Japanese living abroad (48, 50), several others in Europe [United Kingdom (31, 40), Italy (32), Finland (43, 46, 54) and the Netherlands (47)], two in the United States (29, 45), and one in New Zealand (59). International comparative studies included population samples from 13 (37), 4 (60), and 2 (42) nations, respectively. The period of pepsinogen-based studies started about 20 years later than the gastroscopy based studies, with the first pepsinogen-based prevalence study being published by Krasinski et al. (29) in 1986. Studies measuring serum pepsinogen levels, which are both less invasive and less costly than gastroscopy-based screening, mostly included much larger study populations. The smallest sample comprised 105 persons, and eight studies, six studies, and two studies included between 500 and 1,000, between 1,000 and 10,000, or even >10,000 persons, respectively. Most of the studies included both genders, eight studies were restricted to males. The age of participants that were included varied considerably among the different studies. Some studies investigated people with broad age ranges, such as from 20 to 86 years, but much narrower age ranges were included in other studies, such as age groups 25 to 34 and 55 to 64 years, which were included in the largest international comparative study (37).

Prevalences determined in the pepsinogen-based studies may be influenced by factors that modify pepsinogen levels, and prevalences are comparable only as far as identical cut points are used. The very low prevalences found in the EUROGAST study (37), an international comparative study, including 17 populations from 13 countries, primarily reflect the very restrictive cut point used in this study (PGI < 25 ng/mL), which delineates quite severe forms of CAG. Apart from Algeria, prevalences of severe CAG were below 5% in age groups 25 to 34 in all countries included in this study, but ranged up to 11% in age group 55 to 64. Prevalences were higher in Algeria (10.4% and 16.0% in age groups 25 to 34 and 55 to 64, respectively) and Japan than in European and U.S. populations, and there was major variation even within different populations from Japan. Much higher prevalences delineating less severe forms of CAG were found in studies with less restrictive pepsinogen cut points of CAG. An increase of prevalence with age was observed by most of the studies. Most studies did not detect relevant differences in gender, even after stratification by age. Interestingly, the multicenter EUROGAST study (37) detected a higher (or equal) prevalence for women in all 17 populations except for Italy and one population in Japan, but these mostly small differences have to be interpreted with caution given the relatively low number of subjects within the populations. This study is also the only pepsinogen-based study that analyzed age-specific differences by sex, and it found a significantly increased prevalence for women versus men (P = 0.002) in the age group of 25 to 34 but not in the age group of 55 to 64 years (all nations combined).

Time trends in prevalence of CAG can only be judged from studies applying the same methodology in comparable samples of participants from the same country/region at various points of time. Such pepsinogen-based studies were reported by Kobayashi et al. (55) conducted in Japan in 1989/1990 and 1996, respectively, and revealed a decrease in age-specific CAG prevalences over time.

H. pylori infection in the study population was determined in four gastroscopy-based studies (24, 25, 27, 28) and in 17 pepsinogen-based studies (34, 35, 37, 40, 42-44, 47-53, 56, 58, 60). However, only the minority of them reported the prevalence of CAG by H. pylori infection.


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Appendix 1
 References
 
Although CAG is an important step in the development of intestinal gastric cancer, data on prevalence are rare and even lacking entirely for most countries of the world. Due to selection of study samples, to varying definitions of CAG used and to differing cutoff values available, results are difficult to compare even among the few studies reported to date. Nevertheless, it becomes clear that CAG is relatively common among the elderly population. In addition, strong variations between populations and population groups, with much higher rates in some Chinese and Japanese populations than in other parts of the world, as well as an increase with age and the absence of differences between males and females were detectable throughout.

The absence of differences by sex is surprising because men have an increased rate of gastric cancer compared with women (1, 19). Interestingly, reported prevalences even tended to be higher in women in the international EUROGAST study (37). However, this difference in gender seemed to be partly due to body weight and disappeared after adjusting for it (37). Furthermore, in a study by Sipponen et al., the risk of developing gastric cancer was shown to be much smaller for women with CAG than for men with CAG (61). The increase in CAG with age may reflect progression of gastritis with age. However, it may also reflect a birth cohort effect, as pointed out by Sipponen (62): H. pylori gastritis is a birth cohort-related phenomenon, with different cohorts showing different prevalences. Higher CAG prevalences in cohorts born in the beginning of the century than in those born later may thus be caused by a decline in infection with H. pylori in younger birth cohorts. The much higher rates of CAG reported from Asian populations may also be related to the very high prevalence of H. pylori infection found in these countries (63, 64). Likewise, the decrease in age-specific CAG prevalence over time suggested by a study from Japan (55) may be related to decreasing H. pylori prevalences in younger birth cohorts.

A most crucial aspect in studying the epidemiology of CAG is the type of ascertainment of the diagnosis. In the history of screening for atrophic gastritis, several other methods and markers have also been tested, such as measurement of serum gastrin (65, 66), acid secretion (9), the Azure-A test (67), uropepsin determination (67), and investigation of mucins (2, 3) or multiple serum nutrient levels (68). However, only microscopic histologic assessment and serum pepsinogen measurement (occasionally in combination with H. pylori serology) are widely used today.

Considering gastroscopy with subsequent histologic investigation of biopsies, the grading scheme used for defining gastritis has to be taken into account. The Sydney system (69-71) and the Whitehead classification (72, 73) are used most frequently, but a number of authors included in this review also applied other criteria (11, 22, 28, 74-78). Knowledge about the method of extraction of biopsies (blind or under view) and number and location of biopsy sites is of great importance because these aspects have a major influence on results as shown by Kimura et al. (79) and Satoh et al. (80). Unfortunately, the few reported studies showed quite substantial variation in biopsy sites. Optimal biopsy quality and proper orientation are further prerequisites for reliable grading (81), and even the two sides of a biopsy may lead to different results (intrabiopsy variability; ref. 82).

Although biopsy via gastroscopy is often considered to be the gold standard for diagnosing CAG, definition and usage of the terms "atrophic gastritis" and "gastric atrophy" (83-85) are often inconsistent and intraobserver and interobserver variation concerning presence and severity of atrophy is rather large (86). This is true both for pathologists using individual criteria (87) and for those relying on general criteria of the (original and updated) Sydney system (81, 88-90), partly caused by their training in different cultures (Asia and Western countries) with different working hypotheses (85). A new classification and scoring system published in 2002 by Rugge et al. (85, 91) and a morphometric assessment of antral atrophy (92) yet have to be validated. Apart from these difficulties, the procedure of biopsy sampling via gastroscopy is rather unpleasant. Although the feasibility of population-based gastroscopy screenings has been proven in areas of high risk for H. pylori, CAG, and gastric cancer, such as Iran (28), China (22), and Columbia (19), the realization of such large-scale screenings seems unlikely in Western countries with a low risk for CAG and gastric cancer.

In contrast, screenings based on pepsinogen measurements, which are both less expensive and less invasive, have been conducted successfully in several European countries (31, 32, 40, 43, 46, 47, 54). In Japan, about five million people are screened annually for gastric cancer by X-rays (93). In this high-risk country, measurement of serum pepsinogen concentrations may provide an opportunity to include larger proportions of the population in stomach cancer examination programs (94).

The use of a number of different definitions and cutoff values limits comparability of studies relying on pepsinogen concentrations. Early studies establishing cutoff values were conducted by Samloff et al. (9) in 1982 and Miki et al. in 1987 (95) and 1989 (96). In most studies included in this review, CAG was defined by a combination of the PG I concentration and the ratio of PG I to PG II. However, some studies relied solely on the PG I concentration (measuring exclusively corpus atrophy), and some others relied solely on the PG I/PG II ratio. Furthermore, the cutoff values widely differed among the studies: 70 ng/mL (indicating mild, moderate, and severe CAG) was most frequently used as PG I threshold, but there are also studies using 17, 20, or 25 ng/mL (indicating exclusively severe CAG) and one study each with 30, 49, and 50 ng/mL, a pattern that inevitably leads to differences in prevalence estimates. In contrast, the threshold for the PG I/PG II ratio was 3.0 (or 2.9) mostly, but a threshold of 1.3, 1.6, 2.0, and 2.5 was also used in single studies (40, 42, 47, 49, 58).

Specificity and sensitivity of the CAG diagnosis via serum pepsinogen concentrations have been investigated in numerous studies. Samloff et al. (9) predicted the correct mucosal status in 70% of biopsies according to his established cutoff values. Dinis-Ribeiro et al. (10) published a meta-analysis on the validity of pepsinogen tests in 2004 and found that a combination of both PG I and PG I/PG II ratio was required to achieve homogenous high levels of sensitivity and specificity. It is important to bear in mind that all validations refer to comparison with gastroscopy and histologic assessment, which itself cannot claim to be free of inaccuracy. A possible drawback of pepsinogen levels is their possible dependence of additional factors that are difficult to identify. Several studies have shown that smoking elevates both the PG I level and the PG I/PG II ratio (97), and this effect seems to depend on the status of H. pylori infection (98). The influence of alcohol is not yet clear (97). Interestingly, pepsinogen concentrations measured in some parts of Asia partly seem to be higher in general than those in Western countries: in Linqu (China) where CAG is virtually universal, median PG I levels exceeded 90 ng/mL (probably not due to assay procedures; ref. 23), whereas they are usually below 70 ng/mL in European countries (99). Furthermore, the only pepsinogen-based study from China included in this review would suggest much lower CAG prevalences than the multiple gastroscopy-based studies from this country. Different patterns of location and spread of CAG have been forwarded as possible explanations and may compromise the use of pepsinogen levels for international comparative studies.

In this review, only studies published as full articles were included. Most likely, additional results have been presented at conferences and published as meeting proceedings, but the lack of detail and accessibility of pertinent publications would not have allowed comparably detailed presentation of methods and results of those studies in this review.

In conclusion, despite the limited number and comparability of studies, this review indicates that CAG is relatively common among older adults in different parts of the world, but large variations exist. Particularly high prevalences even among younger adults are found in some high-risk regions of gastric cancer in Asia. Large-scale international comparative studies with standardized methodology to determine CAG are needed to provide a more coherent and complete picture of the epidemiology of CAG. Noninvasive measurements of CAG by combined measurement of PG I and the PG I/PG II ratio and potentially additional serum markers may be particularly suited for population-based studies but may require careful consideration of potentially different patterns of CAG in different parts of the world.


   Appendix 1
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Appendix 1
References
 
Studies excluded from this review because of:

(A) Preselection of the study population
  1. Risk factors for atrophic chronic gastritis in a European population: results of the Eurohepygast study. Gut 2002;50:779-85.
  2. Asaka M, Sugiyama T, Nobuta A, Kato M, Takeda H, and Graham DY. Atrophic gastritis and intestinal metaplasia in Japan: results of a large multicenter study. Helicobacter 2001;6:294-9.
  3. Beales IL, Crabtree JE, Scunes D, Covacci A, and Calam J. Antibodies to CagA protein are associated with gastric atrophy in Helicobacter pylori infection. Eur J Gastroenterol Hepatol 1996;8:645-9.
  4. Chang-Claude J, Raedsch R, Waldherr R, et al. Prevalence of Helicobacter pylori infection and gastritis among young adults in China. Eur J Cancer Prev 1995;4:73-9.
  5. Chen XY, van Der Hulst RW, Shi Y, Xiao SD, Tytgat GN, and Ten Kate FJ. Comparison of precancerous conditions: atrophy and intestinal metaplasia in Helicobacter pylori gastritis among Chinese and Dutch patients. J Clin Pathol 2001;54:367-70.
  6. Dursun M, Yilmaz S, Yukselen V, Kilinc N, Canoruc F, and Tuzcu A. Evaluation of optimal gastric mucosal biopsy site and number for identification of Helicobacter pylori, gastric atrophy and intestinal metaplasia. Hepatogastroenterology 2004;51:1732-5.
  7. Fontham ET, Ruiz B, Perez A, Hunter F, and Correa P. Determinants of Helicobacter pylori infection and chronic gastritis. Am J Gastroenterol 1995;90:1094-101.
  8. Fung WP, Lee SK, and Tye CY. The prevalence of chronic gastritis in patients with gastric ulcer. Aust N Z J Med 1975;5:133-7.
  9. Haruma K, Kamada T, Kawaguchi H, et al. Effect of age and Helicobacter pylori infection on gastric acid secretion. J Gastroenterol Hepatol 2000;15:277-83.
  10. Hu PJ, Li YY, Lin HL, et al. Gastric atrophy and regional variation in upper gastrointestinal disease. Am J Gastroenterol 1995;90:1102-6.
  11. Jaskiewicz K, Louwrens HD. Chronic atrophic gastritis in a population at risk for gastric carcinoma. Anticancer Res 1991;11:835-9.
  12. Kato I, Tominaga S, Ito Y, et al. Atrophic gastritis and stomach cancer risk: cross-sectional analyses. Jpn J Cancer Res 1992;83:1041-6.
  13. Kaur G, Raj SM. A study of the concordance between endoscopic gastritis and histological gastritis in an area with a low background prevalence of Helicobacter pylori infection. Singapore Med J 2002;43:090-2.
  14. Kawaguchi H, Haruma K, Komoto K, Yoshihara M, Sumii K, Kajiyama G. Helicobacter pylori infection is the major risk factor for atrophic gastritis. Am J Gastroenterol 1996;91:959-62.
  15. Kiyohira K, Yoshihara M, Ito M, Haruma K, Tanaka S, Chayama K. Serum pepsinogen concentration as a marker of Helicobacter pylori infection and the histologic grade of gastritis; evaluation of gastric mucosa by serum pepsinogen levels. J Gastroenterol 2003;38:332-8.
  16. Kohlstadt IC, Antunez de Mayolo EA, Ramirez-Icaza C. Parietal cell antibodies among Peruvians with gastric pathologic changes. Gastrointestinal Physiology Working Group. Scand J Gastroenterol 1993;28:973-7.
  17. Lee CH, Bang SH, Lee SK, Song KY, Lee IC. Gene expression profiling reveals sequential changes in gastric tubular adenoma and carcinoma in situ. World J Gastroenterol 2005;11:1937-45.
  18. Matsukura N, Onda M, Tokunaga A, et al. Significance of serum markers pepsinogen I and II for chronic atrophic gastritis, peptic ulcer, and gastric cancer. J Clin Gastroenterol 1993;17 Suppl 1:S146-50.
  19. Mihara M, Haruma K, Kamada T, et al. The role of endoscopic findings for the diagnosis of Helicobacter pylori infection: evaluation in a country with high prevalence of atrophic gastritis. Helicobacter 1999;4:40-8.
  20. Montani A, Sasazuki S, Inoue M, Higuchi K, Arakawa T, and Tsugane S. Food/nutrient intake and risk of atrophic gastritis among the Helicobacter pylori-infected population of northeastern Japan. Cancer Sci 2003;94:372-7.
  21. Motteram R. A biopsy study of chronic gastritis and gastric atrophy. J Pathol Bacteriol 1951;63:389-94.
  22. Munoz N, Vivas J, Buiatti E, Kato I, Oliver W. Chemoprevention trial on precancerous lesions of the stomach in Venezuela: summary of study design and baseline data. IARC Sci Publ 1996;125-33.
  23. Ohkuma K, Okada M, Murayama H, et al. Association of Helicobacter pylori infection with atrophic gastritis and intestinal metaplasia. J Gastroenterol Hepatol 2000;15:1105-12.
  24. Oksanen A, Sipponen P, Miettinen A, Sarna S, Rautelin H. Evaluation of blood tests to predict normal gastric mucosa. Scand J Gastroenterol 2000;35:791-5.
  25. Potet F, Florent C, Benhamou E, et al. Chronic gastritis: prevalence in the French population. CIRIG. Gastroenterol Clin Biol 1993;17:103-8.
  26. Primignani M, Agape D, Ronchi G, et al. Gastric histology and function tests in Italian patients with dermatitis herpetiformis. Scand J Gastroenterol 1990;25:357-62.
  27. Ricci C, Vakil N, Rugge M, et al. Serological markers for gastric atrophy in asymptomatic patients infected with Helicobacter pylori. Am J Gastroenterol 2004;99:1910-5.
  28. Ricuarte O, Gutierrez O, Cardona H, Kim JG, Graham DY, El-Zimaity HM. Atrophic gastritis in young children and adolescents. J Clin Pathol 2005;58:1189-93.
  29. Rugge M, Busatto G, Cassaro M, et al. Patients younger than 40 years with gastric carcinoma: Helicobacter pylori genotype and associated gastritis phenotype. Cancer 1999;85:2506-11.
  30. Rugge M, Cassaro M, Leandro G, et al. Helicobacter pylori in promotion of gastric carcinogenesis. Dig Dis Sci 1996;41:950-5.
  31. Ruiz B, Correa P, Fontham ET, Ramakrishnan T. Antral atrophy, Helicobacter pylori colonization, and gastric pH. Am J Clin Pathol 1996;105:96-101.
  32. Satoh K, Kimura K, Sipponen P. Helicobacter pylori infection and chronological extension of atrophic gastritis. Eur J Gastroenterol Hepatol 1995;7 Suppl 1:S11-5.
  33. Shimoyama T, Fukuda S, Tanaka M, Mikami T, Saito Y, Munakata A. High prevalence of the CagA-positive Helicobacter pylori strains in Japanese asymptomatic patients and gastric cancer patients. Scand J Gastroenterol 1997;32:465-8.
  34. Sipponen P, Helske T, Jarvinen P, Hyvarinen H, Seppala K, Siurala, M. Fall in the prevalence of chronic gastritis over 15 years: analysis of outpatient series in Finland from 1977, 1985, and 1992. Gut 1994;35:1167-71.
  35. Sipponen P, Samloff IM, Saukkonen M, Varis K. Serum pepsinogens I and II and gastric mucosal histology after partial gastrectomy. Gut 1985;26:1179-82.
  36. Sitas F, Smallwood R, Jewell D, et al. Serum anti-Helicobacter pylori IgG antibodies and pepsinogens A and C as serological markers of chronic atrophic gastritis. Cancer Epidemiol Biomarkers Prev 1993;2:119-23.
  37. Sobala GM, Pignatelli B, Schorah CJ, et al. Levels of nitrite, nitrate, N-nitroso compounds, ascorbic acid and total bile acids in gastric juice of patients with and without precancerous conditions of the stomach. Carcinogenesis 1991;12:193-8.
  38. Stahel E, Gyr K, Jallah E, Heitz P. Gastroduodenitis and peptic ulcer in a rural Liberian community. An endoscopic prospective study. Trop Geogr Med 1981;33:155-60.
  39. Suriani R, Venturini I, Taraglio S, et al. Type III intestinal metaplasia, Helicobacter pylori infection and gastric carcinoma risk index in an Italian series of 1750 patients. Hepatogastroenterology 2005;52:285-8.
  40. Tamm A, Villako K, Harkonen M, Karonen SL. Serum pepsinogen I and the state of gastric mucosa in an Estonian population sample. Scand J Gastroenterol 1984;19:1091-4.
  41. Tatsuta M, Iishi H, Nakaizumi A, et al. Fundal atrophic gastritis as a risk factor for gastric cancer. Int J Cancer 1993;53:70-4.
  42. Topal D, Goral V, Yilmaz F, Kara IH. The relation of Helicobacter pylori with intestinal metaplasia, gastric atrophy and BCL-2. Turk J Gastroenterol 2004;15:149-55.
  43. Varis O, Valle J, Siurala M. Is Helicobacter pylori involved in the pathogenesis of the gastritis characteristic of pernicious anaemia? Comparison between pernicious anaemia relatives and duodenal ulcer relatives. Scand J Gastroenterol 1993;28:705-8.
  44. Zaitoun AM. Histological study of chronic gastritis from the United Arab Emirates using the Sydney system of classification. J Clin Pathol 1994;47:810-5.

(B) Size of the study population
  1. Andrews GR, Haneman B, Arnold BJ, Booth JC, Taylor K. Atrophic gastritis in the aged. Australas Ann Med 1967;16:230-5.
  2. Earlam RJ, Amerigo J, Kakavoulis T, Pollock DJ. Histological appearances of oesophagus, antrum and duodenum and their correlation with symptoms in patients with a duodenal ulcer. Gut 1985;26:95-100.
  3. Palmer ED. The state of the gastric mucosa of elderly persons without upper gastrointestinal symptoms. J Am Geriatr Soc 1954;2:171-3.
  4. Russell PK, Aziz MA, Ahmad N, Kent TH, Gangarosa EJ. Enteritis and gastritis in young asymptomatic Pakistani men. Am J Dig Dis 1966;11:296-306.


   Footnotes
 
Grant support: German Research Foundation (DFG) within the framework of the Graduiertenkolleg 793.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 12/12/05; revised 3/13/06; accepted 3/29/06.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Appendix 1
 References
 

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