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Is there a link between upper gastrointestinal polyps and colonic polyps? A retrospective study from a Turkish cohort

EXISTE CONEXÃO ENTRE PÓLIPOS GASTROINTESTINAIS PROXIMAIS E PÓLIPOS COLÔNICOS? ESTUDO RETROSPECTIVO DE UMA COORTE TURCA

Abstracts

OBJECTIVE:

To investigate the incidence and associated demographical and clinical factors related to lower GI polyps and neoplasms in patients with upper GI polyps and neoplasms.

METHODS:

We investigated 99 patients who had upper GI polyps and neoplasms and who were screened with colonoscopy: the following data were collected: demographical and clinical data consisting of age, sex, smoking status, presence of H. pylori infection, placement of upper GI polyps or neoplasms, presence of gastric atrophy, usage of proton pump inhibitors (PPI), presence of lower GI polyp or neoplasm, type of colon polyp, pathological grade of colon polyp. The patients were grouped according to having/not having lower GI polyps and neoplasms; data was compared between groups.

RESULTS:

Smoking rate was significantly higher in patients with lower GI polyps and neoplasms (χ2: 4.35, p: 0.03). Furthermore, there was a signifant association between presence of lower GI polyps and neoplasms vs. smoking (OR: 2.44 CI: 1.01-5.84, p: 0.04).

CONCLUSIONS:

Patients with upper GI polyps and neoplasms who are smokers should be considered as candidates for having lower GI polyps and neoplasms and should be screened and followed more carefully. Additionally, we believe that large sampled and prospective studies are needed to higligt the association between upper GI polyps and presence of lower GI polyps and neoplasms.

KEYWORDS:
Gastric polyps; Colon polyps; Risc factor; Retrospective


OBJETIVO:

investigar a incidência, demografia associada e fatores clínicos relativos a pólipos e neoplasias gastrointestinais distais em pacientes com pólipos e neoplasias do trato gastrointestinal superior.

MÉTODOS:

Foram investigados 99 pacientes que apresentaram pólipos ou neoplasias gastrointestinais superiores selecionados através de colonoscopia: os seguintes dados foram coletados: dados demográficos e clínicos consistentes em idade, sexo, tabagismo, presença de infecção por H. pylori, a presença de pólipos ou neoplasias gastrointestinais proximais, presença de atrofia gástrica, uso de inibidores da bomba de prótons (IBP), presença de pólipo ou neoplasia gastrointestinal distal, tipo de pólipo de cólon, grau patológico de pólipo de cólon. Os pacientes foram agrupados de acordo com ter/não ter pólipos ou neoplasias distais; os dados foram comparados entre os grupos.

RESULTADOS:

A taxa de tabagismo foi significativamente maior nos pacientes com pólipos e neoplasias distais (χ2: 4.35, p: 0,03). Além disso houve uma associação significante entre a presença de pólipos e neoplasias distais e tabagismo (OR: 2,44 CI: 1,01-5,84, p: 0,04).

CONCLUSÕES:

Os pacientes fumantes com pólipos e neoplasias do trato gastrointestinal superior devem ser considerados candidatos a pólipos e neoplasias distais e devem ser rastreados e seguidos com mais cuidado. Adicionalmente, grandes amostras e estudos prospectivos são necessários para esclarecer a associação entre pólipos gastrointestinais superiores e a presença de pólipos e neoplasias gastrointestinais distais.

PALAVRAS-CHAVE:
pólipos gástricos; pólipos no cólon; fator de risco; estudos retrospectivos


INTRODUCTION

Colorectal cancers are among the most prevalent cancer types worldwide in both male and female.11 Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin. 2010; 60(5):277-300. http://dx.doi.org/.3322/caac.20073
http://dx.doi.org/.3322/caac.20073...
It is estimated that colorectal cancers are the third cause of death in the general population.22 Hawkins NJ, Ward RL. Sporadic colorectal cancers with microsatellite instability and their possible origin in hyperplastic polyps and serrated adenomas. J Natl Cancer Inst. 2001; 93(17):1307-13. http://dx.doi.org/10.1093/jnci/93.17.1307
http://dx.doi.org/10.1093/jnci/93.17.130...
,33 Jass JR. Hyperplastic-like polyps as precursors of microsatellite-unstable colorectal cancer. Am J Clin Pathol. 2003; 119(6):773-5. http://dx.doi.org/10.1309/UYN70N9W2DVN9ART
http://dx.doi.org/10.1309/UYN70N9W2DVN9A...
Early detection of malignant colon polyps and removal of them may decrease mortality.44 Kahi CJ, Imperiale TF, Juliar BE, Rex DK. Effect of screening colonoscopy on colorectal cancer incidence and mortality. Clin Gastroenterol Hepatol. 2009;7(7):770-5. http://dx.doi.org/10.1016/j.cgh.2008.12.030
http://dx.doi.org/10.1016/j.cgh.2008.12....

5 Levin B, Lieberman DA, McFarland B, Smith RA, Brooks D, Andrews KS, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. CA Cancer J Clin. 58(3)130-60. http://dx.doi.org/10.3322/CA.2007.0018
http://dx.doi.org/10.3322/CA.2007.0018...
-66 Winawer SJ, Zauber AG, Ho MN, O'Brien MJ, Gottlieb LS, Sternberg SS, et al. Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup. N Engl J Med. 1993; 329(27):1977-81. http://dx.doi.org/10.1056/NEJM199312303292701
http://dx.doi.org/10.1056/NEJM1993123032...

Patients with upper gastrointestinal (GI) polyps and neoplasms might have synchronous and metachronous polyps or neoplasms in lower GI tract, such as the rectum and the colon. The etiology of this coexistence still remains unclear. Possible explanations refer to genetic factors such as p 53, K-Ras, APC, etc.77 Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, et al. Genetic alterations during colorectal-tumor development. N Engl J Med. 1988;319(9):525-32. http://dx.doi.org/10.1056/NEJM198809013190901
http://dx.doi.org/10.1056/NEJM1988090131...

8 Ohtani H, Yashiro M, Onoda N, Nishioka N, Kato Y, Yamamoto S, et al. Synchronous multiple primary gastrointestinal cancer exhibits frequent microsatellite instability. Int J Cancer. 2000; 86(5):678-83. http://dx.doi.org/10.1002/(SICI)1097-0215(20000601)86:53.0.CO;2-O
http://dx.doi.org/10.1002/(SICI)1097-021...
-99 Schulmann K, Reiser M, Schmiegel W. Colonic cancer and polyps. Best Pract Res Clin Gastroenterol. 2000;16(1):91-114. http://dx.doi.org/10.1053/bega.2002.0268
http://dx.doi.org/10.1053/bega.2002.0268...
Others are enviromental factors such as H.pylori infection, smoking and some additional factors.1010 Calonge N, Petitti DB, DeWitt TG, Dietrich AJ, Gregory KD, Harris R, et al. Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2008;149(9):627-37. Because of this possible coexistence, the patients with upper GI polyps and neoplasms are recommended for screening their lower GI tract in terms of polyps and neoplasms. However, there is still no standard strategy, accepted for patients with upper GI polyps, to screen for colonic neoplasms as well as colonic polyps.

In this study we aimed to investigate the incidence of lower GI poyps and neoplasms and to research associated factors in patients in whom upper GI polyps and neoplasms were detected.

METHODS

In present study we screened retrospectively the clinical records of 99 patients with upper GI polyps, whose diagnosis had been confirmed histopathologically by the same patologist, who were admitted to the Turgut Özal University Department of Gastroenterology between January 2011 and December 2013. Of 798 patients with upper GI polyps 600 patients were excluded because they had not undergone colonoscopy; 50 patients were excluded because of insufficent data; 39 patients were not included becasue they had no upper GI polyps or neoplasms. After these exclusions, 99 patients were included in the study. The collected clinical data consisted of: age, sex, smoking status, the presence of H. pylori Infection, anatomical location of upper GI polyps or neoplasms, presence of gastric atrophy, usage of proton pump inhibitors (PPI), presence of lower GI polyp or neoplasm, subtype of colonic polyp such as hyperplastic, adenomatous or neoplastic, pathological grade of colon polyp such as absence of dysplasia, low grade dysplasia, high grade dysplasia.

Statistical Method

All data were evaluated through the Statistical Package for the Social Sciences, PC version 17.0 (SPSS, Chicago, IL). Confidence intervals (CI) of 95% and a 2-tailed P value of less than 0.05 were accepted to be statistically significant for all analyses. Numerical variables were tested for homogenity of variance using the Levene test and for normality of distribution by the Kolmogorov-Smirnov test. Categorical variables were analyzed through the χ22 Hawkins NJ, Ward RL. Sporadic colorectal cancers with microsatellite instability and their possible origin in hyperplastic polyps and serrated adenomas. J Natl Cancer Inst. 2001; 93(17):1307-13. http://dx.doi.org/10.1093/jnci/93.17.1307
http://dx.doi.org/10.1093/jnci/93.17.130...
test.

A series of logistic regressions examined the strength of associations between the presence of colon polyps (dependent variable) and age, sex, smoking status, the presence of H. pylori Infection, anatomical location of upper GI polyps or neoplasms, presence of gastric atrophy, usage of proton pump inhibitors (PPI). Results are presented as adjusted odds ratios (ORs) for independent variables of interest with associated 95% confidence intervals (CIs).

RESULTS

Ninety-nine patients with upper GI polyps or neoplasms were included to the study. The mean age of participants was 59.18 ± 13.28 years. Forty patients were male (40.4%), 59 female (59.6%). Table 1. Presents general information on the included patients

Table 1
Comparison of demographical and clinical parameters between groups.

Table 2 shows the characteristics of the polyps and neoplasms found in the upper gastrointestinal tract of the included patients. It also shows the various indications for the gastroduodenoscopy procedures which led to the findings of the polyps and neoplasms. Polyps/neoplasms located in the stomach were evenly distributed between fundus, corpus and antrum; only four lesions were found in the duodenum. A vast majority of the lesions were hyperplastic polyps. Only three instances of adenocarcinoma were detected.

Table 2
Position and types of Upper Gastro-IntestinaI tract polyps and neoplasms.

Table 3 shows that 47 out of the 99 patients with upper gastrointestinal tract polypsor neoplasia also presented lower gastrointestinal polyps or neoplasia. Hyperplastic polyps were again the most frequent type of lesion.

Table 3
Occurrence and types of lower Gastrointestinal tract polyps and neoplasms

The patients were compared in terms of demographical and clinical characteristics as to whether they had lower GI polyps or neoplasms. The smoking rate was significantly higher in patients with GI polyps or neoplasms (c22 Hawkins NJ, Ward RL. Sporadic colorectal cancers with microsatellite instability and their possible origin in hyperplastic polyps and serrated adenomas. J Natl Cancer Inst. 2001; 93(17):1307-13. http://dx.doi.org/10.1093/jnci/93.17.1307
http://dx.doi.org/10.1093/jnci/93.17.130...
: 4.35, p: 0.03). The other comparisons of sociodemographic and clinical characteristic of groups were found to be non significant (p>0.05).

A logistic regression model examined associations between presence of colon polyps or neoplasms (dependent variable) and gender, age, histology of gastric mucosa, H. pylori infection, presence of gastric atrophy and usage of PPIs. There was a significant association between presence of lower GI polyps or neoplasms and smoking (OR: 2.44 CI: 1.01-5.84, p: 0.04), as shown in Table 4.

Table 4
Logistic regression analysis of presence of lower gastrointestinal system or neoplasms. Significant p values are displayed in bold character

DISCUSSION

In present study, the most important finding is the significant association between presence of lower GI polyps or neoplasms and smoking.

The mechanisms underlying the coincidence of upper GI polyps or neoplasms and lower GI polyps and neoplasms is complex and not completely elucidated. As aforementioned, the etiology of this coincidence may be related with genetics as well as with some environmental factors.1111 Wu ZJ, Lin Y, Xiao J, Wu LC, Liu JG. Clinical Significance of Colonoscopy in Patients with Upper Gastrointestinal Polyps and Neoplasms: A Meta Analysis. PLoS ONE. 2014;9(3):e91810. http://dx.doi.org/10.1371/journal.pone.0091810
http://dx.doi.org/10.1371/journal.pone.0...
Evidence derived from epidemiologic studies supports this correlation: investigators have reported that patients who had colonic polyposis syndromes had higher incidence of gastric and duodenal polyps;1212 Gu GL, Wang SL, Wei XM, Bai L. Diagnosis and treatment of Gardner syndrome with gastric polyposis: a case report and review of the literature. World J Gastroenterol. 2008;14(13):2121-3. http://dx.doi.org/10.3748/wjg.14.2121
http://dx.doi.org/10.3748/wjg.14.2121...
,1313 Attard TM, Cuffari C, Tajouri T, Stoner JA, Eisenberg MT, Yardley JH, et al. Multicenter experience with upper gastrointestinal polyps in pediatric patients with familial adenomatous polyposis. Am J Gastroenterol. 2004;99(4):681-6. http://dx.doi.org/10.1111/j.1572-0241.2004.04115.x
http://dx.doi.org/10.1111/j.1572-0241.20...
in addition, the risk of colon cancer might be increased in patients who had gastric fundic gland polyps.1414 Teichmann J, Weickert U, Riemann JF. Gastric fundic gland polyps and colonic polyps - is there a link, really? Eur J Med Res. 2008;13(5):192-5. Lee et al. reported that the percentage of colorectal neoplasm in gastric cancer vs. control groups were 35.8% vs. 17.9% , respectively.1515 Lee SS, Jung WT, Kim CY, Ha CY, Min HJ, et al. The synchronous prevalence of colorectal neoplasms in patients with stomach cancer. J Korean Soc Coloproctol. 2011;27(5):246-51. http://dx.doi.org/10.3393/jksc.2011.27.5.246
http://dx.doi.org/10.3393/jksc.2011.27.5...
Park et al. also reported higher colorectal adenoma and colorectal cancer in patients with gastric cancer compared to control group.1616 Park SR, Hong YS, Lim HS, Seong MW, Kong SY, et al. Phase I clinical and pharmacokinetic/pharmacogenetic study of a triplet regimen of S-1/irinotecan/oxaliplatin in patients with metastatic colorectal or gastric cancer. Cancer Chemother Pharmacol. 2013;72(5):953-64. http://dx.doi.org/10.1007/s00280-013-2272-0
http://dx.doi.org/10.1007/s00280-013-227...
In the present study, 52 patients were found to have lower GI polyps or neoplasms (52.5%). When compared with previous studies, the presence of lower GI polyps and neoplasms was higher in patients with upper GI polyps. It is possible that the high percentage reported in this study might be due to the small sample size of the present study.

As aforementioned, patients who had gastric fundic gland polyps were reported to have increased risk for presence of colorectal cancer.1414 Teichmann J, Weickert U, Riemann JF. Gastric fundic gland polyps and colonic polyps - is there a link, really? Eur J Med Res. 2008;13(5):192-5. In the present study, 21 patients had fundic gland polyps and most of them had hyperplastic polyps of upper GI system. However, the incidence of lower GI polyps and neoplasms did not differ significantly according to the type of gastric polyps. Some studies reported a link between H. pylori infection and colon polyps and neoplasms.1515 Lee SS, Jung WT, Kim CY, Ha CY, Min HJ, et al. The synchronous prevalence of colorectal neoplasms in patients with stomach cancer. J Korean Soc Coloproctol. 2011;27(5):246-51. http://dx.doi.org/10.3393/jksc.2011.27.5.246
http://dx.doi.org/10.3393/jksc.2011.27.5...

16 Park SR, Hong YS, Lim HS, Seong MW, Kong SY, et al. Phase I clinical and pharmacokinetic/pharmacogenetic study of a triplet regimen of S-1/irinotecan/oxaliplatin in patients with metastatic colorectal or gastric cancer. Cancer Chemother Pharmacol. 2013;72(5):953-64. http://dx.doi.org/10.1007/s00280-013-2272-0
http://dx.doi.org/10.1007/s00280-013-227...

17 Zhang Y, Gao C, Zhai JH. Meta-analysis on the relationship between colorectal cancer and Helicobacter pylori infection. Zhonghua Liu Xing Bing Xue Za Zhi. 2009;30(1):73-7.
-1818 Zhao YS, Wang F, Chang D, Han B, You DY: Meta-analysis of different test indicators: Helicobacter pylori infection and the risk of colorectal cancer. Int J Colorectal Dis. 2008;23(9):875-82. http://dx.doi.org/10.1007/s00384-008-0479-z
http://dx.doi.org/10.1007/s00384-008-047...
However, other studies reported no association between H. pylori infection and lower GI polyps and neoplasms.1919 Limburg PJ, Stolzenberg-Solomon RZ, Colbert LH, Perez-Perez GI, Blaser MJ, Taylor PR, et al. Helicobacter pylori seropositivity and colorectal cancer risk: a prospective study of male smokers. Cancer Epidemiol Biomarkers Prev. 2002; 11(10 Pt 1):1095-9.

20 Moss SF, Neugut AI, Garbowski GC, Wang S, Treat MR, Forde KA. Helicobacter pylori seroprevalence and colorectal neoplasia: evidence against an association. J Natl Cancer Inst. 1995;87(10):762-3. http://dx.doi.org/10.1093/jnci/87.10.762
http://dx.doi.org/10.1093/jnci/87.10.762...

21 Robertson DJ, Sandler RS, Ahnen DJ, Greenberg ER, Mott LA, Cole BF, et al. Gastrin, Helicobacter pylori, and colorectal adenomas. Clin Gastroenterol Hepatol. 2009;7(2):163-167. http://dx.doi.org/10.1016/j.cgh.2008.09.006
http://dx.doi.org/10.1016/j.cgh.2008.09....
-2222 Siddheshwar RK, Muhammad KB, Gray JC, Kelly SB. Seroprevalence of Helicobacter pylori in patients with colorectal polyps and colorectal carcinoma. Am J Gastroenterol. 2001;96(1):84-8. Furthermore, a meta-analysis concluded that there is no association between H. pylori infection and colon polyps or neoplasms.1111 Wu ZJ, Lin Y, Xiao J, Wu LC, Liu JG. Clinical Significance of Colonoscopy in Patients with Upper Gastrointestinal Polyps and Neoplasms: A Meta Analysis. PLoS ONE. 2014;9(3):e91810. http://dx.doi.org/10.1371/journal.pone.0091810
http://dx.doi.org/10.1371/journal.pone.0...
In present study, no association was found between H. pylori infection and lower GI polyps or neoplasms. Our finding agrees with reported data negating a link between H. pylori infection and colonic polyps.1111 Wu ZJ, Lin Y, Xiao J, Wu LC, Liu JG. Clinical Significance of Colonoscopy in Patients with Upper Gastrointestinal Polyps and Neoplasms: A Meta Analysis. PLoS ONE. 2014;9(3):e91810. http://dx.doi.org/10.1371/journal.pone.0091810
http://dx.doi.org/10.1371/journal.pone.0...
,1414 Teichmann J, Weickert U, Riemann JF. Gastric fundic gland polyps and colonic polyps - is there a link, really? Eur J Med Res. 2008;13(5):192-5.

Patients with lower GI polyps and neoplasms had similar incidence of gastric atrophy compared to patients with no lower GI polyps and neoplasms. To the best of our knowledge, there is no report linking gastric atrophy and colon polyps.

Only one study by Hsu et al.2323 Hsu WH, Wu IC, Kuo CH, Su YC, Lu CY, Kuo FC, et al. Influence of proton pump inhibitor use in gastrointestinal polyps. Kaohsiung J Med Sci. 2010;26(2):76-83. investigated the association between the use of proton pump inhibitors and colon polyps; no association was reported; similarly, we found no differences between groups in terms of PPI treatment. We suggest that further studies are needed to investigate whether there is a link between PPI treatment and colon polyps. We also failed to demonstrate a significant difference between groups in terms of placement of upper GI polyps and neoplasms. In the literature, there was no noteworthy association between placement of upper GI polyps and neoplasms and colon polyps.

A meta-analysis which investigated the association between smoking and colorectal cancers reported a link between smoking and colorectal cancers.2424 Botteri E, Iodice S, Raimondi S, Maisonneuve P, Lowenfels AB. Cigarette smoking and adenomatouspolyps: a meta-analysis. Gastroenterology. 2008;134(2):388-95. http://dx.doi.org/10.1053/j.gastro.2007.11.007
http://dx.doi.org/10.1053/j.gastro.2007....
Smoking has also been considered as a well-established risk factor of colon neoplasms. In our study, the rate of smoking was found to be significantly higher in patients with lower GI polyps and neoplasms. Furthermore, there was a significant association between smoking status and presence of lower GI polyps and neoplasms.

Our study has a limitation: the numbers of participants might be considered low for a retrospective study. This limitation is due to the inclusion criteria of the study. We consider that further and prospective studies are needed for comparing patients with and without upper GI polyps and neoplasms.

In conclusion, we suggest that patients who had upper GI polyps and neoplasms should be screened carefully for the presence GI polyps and neoplasms. Particularly, patients with upper GI polyps and neoplasms who are smokers should be considered as candidates for having lower GI polyps and neoplasms and should be screened and followed up more carefully. Further, large sampled and prospective studies are needed to highlight the association between upper GI polyps and presence of lower GI polyps and neoplasms.

REFERENCES

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  • 2
    Hawkins NJ, Ward RL. Sporadic colorectal cancers with microsatellite instability and their possible origin in hyperplastic polyps and serrated adenomas. J Natl Cancer Inst. 2001; 93(17):1307-13. http://dx.doi.org/10.1093/jnci/93.17.1307
    » http://dx.doi.org/10.1093/jnci/93.17.1307
  • 3
    Jass JR. Hyperplastic-like polyps as precursors of microsatellite-unstable colorectal cancer. Am J Clin Pathol. 2003; 119(6):773-5. http://dx.doi.org/10.1309/UYN70N9W2DVN9ART
    » http://dx.doi.org/10.1309/UYN70N9W2DVN9ART
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    Kahi CJ, Imperiale TF, Juliar BE, Rex DK. Effect of screening colonoscopy on colorectal cancer incidence and mortality. Clin Gastroenterol Hepatol. 2009;7(7):770-5. http://dx.doi.org/10.1016/j.cgh.2008.12.030
    » http://dx.doi.org/10.1016/j.cgh.2008.12.030
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    Levin B, Lieberman DA, McFarland B, Smith RA, Brooks D, Andrews KS, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. CA Cancer J Clin. 58(3)130-60. http://dx.doi.org/10.3322/CA.2007.0018
    » http://dx.doi.org/10.3322/CA.2007.0018
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    Winawer SJ, Zauber AG, Ho MN, O'Brien MJ, Gottlieb LS, Sternberg SS, et al. Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup. N Engl J Med. 1993; 329(27):1977-81. http://dx.doi.org/10.1056/NEJM199312303292701
    » http://dx.doi.org/10.1056/NEJM199312303292701
  • 7
    Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, et al. Genetic alterations during colorectal-tumor development. N Engl J Med. 1988;319(9):525-32. http://dx.doi.org/10.1056/NEJM198809013190901
    » http://dx.doi.org/10.1056/NEJM198809013190901
  • 8
    Ohtani H, Yashiro M, Onoda N, Nishioka N, Kato Y, Yamamoto S, et al. Synchronous multiple primary gastrointestinal cancer exhibits frequent microsatellite instability. Int J Cancer. 2000; 86(5):678-83. http://dx.doi.org/10.1002/(SICI)1097-0215(20000601)86:53.0.CO;2-O
    » http://dx.doi.org/10.1002/(SICI)1097-0215(20000601)86:53.0.CO;2-O
  • 9
    Schulmann K, Reiser M, Schmiegel W. Colonic cancer and polyps. Best Pract Res Clin Gastroenterol. 2000;16(1):91-114. http://dx.doi.org/10.1053/bega.2002.0268
    » http://dx.doi.org/10.1053/bega.2002.0268
  • 10
    Calonge N, Petitti DB, DeWitt TG, Dietrich AJ, Gregory KD, Harris R, et al. Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2008;149(9):627-37.
  • 11
    Wu ZJ, Lin Y, Xiao J, Wu LC, Liu JG. Clinical Significance of Colonoscopy in Patients with Upper Gastrointestinal Polyps and Neoplasms: A Meta Analysis. PLoS ONE. 2014;9(3):e91810. http://dx.doi.org/10.1371/journal.pone.0091810
    » http://dx.doi.org/10.1371/journal.pone.0091810
  • 12
    Gu GL, Wang SL, Wei XM, Bai L. Diagnosis and treatment of Gardner syndrome with gastric polyposis: a case report and review of the literature. World J Gastroenterol. 2008;14(13):2121-3. http://dx.doi.org/10.3748/wjg.14.2121
    » http://dx.doi.org/10.3748/wjg.14.2121
  • 13
    Attard TM, Cuffari C, Tajouri T, Stoner JA, Eisenberg MT, Yardley JH, et al. Multicenter experience with upper gastrointestinal polyps in pediatric patients with familial adenomatous polyposis. Am J Gastroenterol. 2004;99(4):681-6. http://dx.doi.org/10.1111/j.1572-0241.2004.04115.x
    » http://dx.doi.org/10.1111/j.1572-0241.2004.04115.x
  • 14
    Teichmann J, Weickert U, Riemann JF. Gastric fundic gland polyps and colonic polyps - is there a link, really? Eur J Med Res. 2008;13(5):192-5.
  • 15
    Lee SS, Jung WT, Kim CY, Ha CY, Min HJ, et al. The synchronous prevalence of colorectal neoplasms in patients with stomach cancer. J Korean Soc Coloproctol. 2011;27(5):246-51. http://dx.doi.org/10.3393/jksc.2011.27.5.246
    » http://dx.doi.org/10.3393/jksc.2011.27.5.246
  • 16
    Park SR, Hong YS, Lim HS, Seong MW, Kong SY, et al. Phase I clinical and pharmacokinetic/pharmacogenetic study of a triplet regimen of S-1/irinotecan/oxaliplatin in patients with metastatic colorectal or gastric cancer. Cancer Chemother Pharmacol. 2013;72(5):953-64. http://dx.doi.org/10.1007/s00280-013-2272-0
    » http://dx.doi.org/10.1007/s00280-013-2272-0
  • 17
    Zhang Y, Gao C, Zhai JH. Meta-analysis on the relationship between colorectal cancer and Helicobacter pylori infection. Zhonghua Liu Xing Bing Xue Za Zhi. 2009;30(1):73-7.
  • 18
    Zhao YS, Wang F, Chang D, Han B, You DY: Meta-analysis of different test indicators: Helicobacter pylori infection and the risk of colorectal cancer. Int J Colorectal Dis. 2008;23(9):875-82. http://dx.doi.org/10.1007/s00384-008-0479-z
    » http://dx.doi.org/10.1007/s00384-008-0479-z
  • 19
    Limburg PJ, Stolzenberg-Solomon RZ, Colbert LH, Perez-Perez GI, Blaser MJ, Taylor PR, et al. Helicobacter pylori seropositivity and colorectal cancer risk: a prospective study of male smokers. Cancer Epidemiol Biomarkers Prev. 2002; 11(10 Pt 1):1095-9.
  • 20
    Moss SF, Neugut AI, Garbowski GC, Wang S, Treat MR, Forde KA. Helicobacter pylori seroprevalence and colorectal neoplasia: evidence against an association. J Natl Cancer Inst. 1995;87(10):762-3. http://dx.doi.org/10.1093/jnci/87.10.762
    » http://dx.doi.org/10.1093/jnci/87.10.762
  • 21
    Robertson DJ, Sandler RS, Ahnen DJ, Greenberg ER, Mott LA, Cole BF, et al. Gastrin, Helicobacter pylori, and colorectal adenomas. Clin Gastroenterol Hepatol. 2009;7(2):163-167. http://dx.doi.org/10.1016/j.cgh.2008.09.006
    » http://dx.doi.org/10.1016/j.cgh.2008.09.006
  • 22
    Siddheshwar RK, Muhammad KB, Gray JC, Kelly SB. Seroprevalence of Helicobacter pylori in patients with colorectal polyps and colorectal carcinoma. Am J Gastroenterol. 2001;96(1):84-8.
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    » http://dx.doi.org/10.1053/j.gastro.2007.11.007

Publication Dates

  • Publication in this collection
    Jul-Aug 2016

History

  • Received
    20 Apr 2016
  • Reviewed
    14 June 2016
  • Accepted
    23 July 2016
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