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Article

Association of Colonic Diverticula with Colorectal Adenomas and Cancer

by
Angelo Viscido
1,†,
Fabiana Ciccone
2,†,
Filippo Vernia
1,
Dolores Gabrieli
2,
Annalisa Capannolo
1,
Gianpiero Stefanelli
1,
Stefano Necozione
3,
Giorgio Valerii
2,
Hassan Ashktorab
4 and
Giovanni Latella
1,*
1
Gastroenterology Unit, Department of Life, Health and Environmental Sciences, University of L’Aquila, 67100 L’Aquila, Italy
2
Gastroenterology Unit, Giuseppe Mazzini Hospital, 64100 Teramo, Italy
3
Epidemiology Unit, Department of Life, Health and Environmental Sciences, University of L’Aquila, 67100 L’Aquila, Italy
4
Department of Medicine and Cancer Center, Howard University College of Medicine, Washington, DC 20059, USA
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Medicina 2021, 57(2), 108; https://doi.org/10.3390/medicina57020108
Submission received: 22 November 2020 / Revised: 19 January 2021 / Accepted: 20 January 2021 / Published: 25 January 2021
Browse Figures
Review Reports Versions Notes

Abstract

:
Background and Objectives: Conflicting evidence is reported regarding any association between colonic diverticula with colorectal adenomas or cancer. The present study aimed to evaluate, in a cohort of Caucasian patients, the association between colonic diverticula and colorectal polyps and cancer. Materials and Methods: All consecutive patients undergoing colonoscopy at our institution were included in the study. The presence and location of diverticula, polyps, and cancers were recorded. Histologically, polyps were classified as adenoma (with low or high dysplasia), hyperplastic, or inflammatory. The relative risk of the association of polyps and cancer with diverticula was assessed. Multiple logistic regression analyses, including age, sex, family history for colorectal cancer (CRC), and family history for diverticula, were carried out. Results: During the study period, 1490 patients were enrolled; 37.2% (n = 555) showed colonic diverticula or polyps or CRC (308 males, mean age 66 years). Particularly, 12.3% (n = 183) patients presented only diverticula, 13.7% (n = 204) only polyps or cancer, 11.3% (n = 168) both diseases, and 62.7% (n = 935) neither diverticula nor polyps and cancer. A total of 38 patients presented colorectal cancer, 17 of which had also diverticula. A significant increase in relative risk (RR 2.81, 95% CI 2.27–3.47, p < 0.0001) of colorectal adenoma and cancer in patients with colonic diverticula was found. At multivariate analysis, only diverticula resulted to be significantly associated with colorectal adenomas and cancer (Odds Ratio, OR 3.86, 95% CI 2.90–5.14, p < 0.0001). Conclusions: A significant association of colonic diverticula with colorectal adenoma or cancer was found. This implies that patients with colonic diverticula require a vigilant follow-up procedure for the prevention of colorectal cancer from those applicable to the general population.

1. Introduction

Colonic diverticula and colorectal polyps and cancer are common findings during colonoscopy, especially in patients over 50 years of age [1]. Most patients with diverticula of the colon remain asymptomatic throughout their lives, a condition commonly referred to as diverticulosis or asymptomatic diverticula. Approximately 20% of those with colonic diverticula develop symptoms (abdominal pain or discomfort, bloating, constipation, or diarrhea), conditions described under the general heading of symptomatic diverticular disease (DD), which may be uncomplicated, recurrent, or complicated [2,3,4]. Symptomatic DD includes the types without inflammation (symptomatic uncomplicated diverticular disease (SUDD)) and those with overt inflammation of the colon, including both segmental colitis associated with diverticula (SCAD) and diverticulitis [5]. This latter form can be acute or chronic, uncomplicated, or complicated.
Patients with colorectal polyps and early colorectal cancer (CRC) are, in most cases, asymptomatic [6,7]. Bowel habit alterations and/or hematochezia appear in a minority of cases and only in the presence of large and multiple polyps or ulcerated and/or stenotic CRC. The screening tests are aimed at detecting asymptomatic polyps and CRC [8,9]. A recent study demonstrated that bleeding-related signs (overt bleeding, iron deficiency anemia, or a positive fecal occult blood test) are present in three-quarters of patients with CRC. Both overt and occult bleeders are less likely than non-bleeders to have metastases at diagnosis. Overt bleeders are very unlikely to present with obstructive symptoms and most occult bleeders are found to have proximal cancer [10].
The prevalence of both diverticula and colorectal neoplasia increases exponentially with age.
Under the age of 40, the frequency of diverticula is estimated at approximately 5%, increasing to 65–70% for those over 65 [11].
CRC is a highly common malignancy in European countries and the world in general [12,13,14].
According to GLOBOCAN data, 1.36 million new cases, affecting 17.2 per 100,000 populations, are diagnosed worldwide each year and 693,000 people die from CRC, amounting to a yearly mortality rate of 8.4 per 100,000 [14]. CRC has become a major public health concern because, despite treatment, as many as half of CRC patients die from the disease [13]. CRC is sporadic in 90% of patients, whereas in <10% it is inherited [15,16] or can be the complication result of inflammatory bowel disease (IBD), either ulcerative colitis (UC) or Crohn’s disease (CD) [17,18,19,20]. In most cases, CRC develops from adenoma, a preclinical benign precursor, the progression from early adenoma to invasive cancer taking years [21]. The estimated CRC lifetime risk is 5–6% with incidence rates increasing sharply after the age of 50 [21,22].
In addition to age, diverticula and colorectal neoplasms appear to share other risk factors, such as a diet low in fibers and rich in saturated fats, obesity, and slow colonic transit time [1,2].
Inflammation also seems to be a common finding shared by the two conditions, the presence of a chronic inflammatory process increasing the risk of a malignant transformation [20,23,24]; chronic microscopic inflammation of the colon has been reported in DD, even in the SUDD [25].
All this evidence gives rise to the hypothesis of a possible association between diverticula and colorectal adenomas and cancer. However, contrasting results have been reported as some studies supporting this thesis [1,26,27,28,29], while others demonstrate an absence of this association [30,31,32]. Most of the evidence available in literature derives from retrospective studies, and the results from the few prospective cohorts are discordant, especially among different ethnic groups. Thus, further prospective studies are needed to establish the real relationship between DD, colorectal polyps, and CRC, as this could have important implications for CRC screening programs. The present study aimed to evaluate, in a cohort of Caucasian patients, the association between colonic diverticula, colorectal polyps, and cancer.

2. Materials and Methods

2.1. Study Population

This prospective study was carried out at the Gastroenterology Unit of the Medical School of the University of L’Aquila, L’Aquila, Italy, and the Gastroenterology Unit, Giuseppe Mazzini Hospital, Teramo, Italy.
All consecutive patients who underwent colonoscopy in the period between September 2016 and September 2019 were included. Patients underwent the procedure for a variety of reasons: uncomplicated lower abdominal pain or discomfort, hematochezia, changes in bowel habit, weight loss, iron-deficiency anemia, chronic constipation, chronic diarrhea, surveillance after colonic polypectomy, and screening for CRC.
Ethics Committee Approval: The study was performed with the institutional review board’s approval (Prot. N. 43958). All clinical investigations were conducted according to the principles laid down in the Declaration of Helsinki.
Informed consent: Written informed consent was obtained from all patients included in the present study.

2.2. Colonoscopy and Histopathology

Before the colonoscopy, patients received a polyethylene glycol solution for bowel preparation and intravenous diazepam or midazolam for sedation. During the study period, 1994 colonoscopies were performed. A total of 504 patients did not meet the inclusion criteria, as 311 were affected by IBD, infectious colitis, or ischemic colitis, 137 had poor bowel cleansing (Boston score 0–1) [33], 54 had incomplete endoscopic examination, and 2 had polyps close to the scar, resulting from previous polypectomies. A total of 1490 patients were therefore enrolled and included in the statistical analysis. All enrolled patients were divided into four groups according to the endoscopic findings: group A, patients with only DD; group B, patients with only polyps or CRC; group C, patients showing both DD and polyps or CRC; and group D, patients without diverticula, polyps, or cancer (Figure 1). Data were recorded on a standard database.
Colonoscopy findings were documented using a standardized colonoscopy-reporting system. Colonic diverticula are characterized by the herniation of the colonic mucosa and submucosa through defects in the muscle layer at the weakest point in the colonic wall. Diverticulosis was defined as the presence of at least two diverticula, in the absence of symptoms. DD was defined as intestinal symptoms and signs related to the presence of colonic diverticula [5,34].
Colorectal polyps were classified according to their location and histopathology. We defined the proximal colon as the cecum, ascending colon, and transverse colon, including splenic flexure, distal colon as descending colon, sigmoid colon, and rectum. All polyps were removed with a forceps biopsy (polyps < 5 mm) or a diathermic loop (polyps > 5 mm), as appropriate. Multiple biopsies were taken from CRC.
Histological samples were classified as cancer, adenoma (with low or high dysplasia), hyperplastic, or inflammatory polyps.

2.3. Statistical Analysis

Comparisons among the groups were assessed by the chi-square test and Fisher’s exact test, as appropriate, for categorical variables. The relative risk (RR), with the 95% confidence intervals of the association of polyps and cancer with diverticula, was assessed. Multiple logistic regression analyses, including age, sex, family history for CRC, and family history for diverticula, were carried out. All statistical analyses were performed using the STATA version 15.1 2017 (StataCorp LLC, College Station, TX, USA).

3. Results

Of the 1490 patients enrolled, 37.2% (555/1490) showed colonic diverticula, polyps, or CRC (308 M, 247 F, mean age 66 years). In particular, 23.5% (351/1490) showed colonic diverticula, 15.0% (224/1490) colorectal adenomas, 2.5% (37/1490) CRC, 6.5% (97/1490) hyperplastic polyps, 0.9% (14/1490) inflammatory polyps, and 62.7% (935/1490) had other different lesions, such as proctitis, angiodysplasia, hemorrhoids, or no mucosal lesions. The study population was divided into four patient groups (Figure 1): Group A: 12.3% patients (183) with only diverticula (52% male vs. 48% female); Group B: 13.7% patients (204) with only polyps or cancers (53% male vs. 47% female); Group C: 11.3% patients (168) with both diverticula and polyps or cancers (62% male vs. 38% female); Group D: 62.7% patients (935) without neoplastic lesions or diverticula (56% male vs. 44% female).
Clinical characteristics of the four groups of patients are summarized in Table 1. Histological characteristics and localization of neoplastic lesions and diverticula of Group C (patients with both polyps or CRC and diverticula) are summarized in Table 2. In this group of patients, most polyps were found in the distal colon.
In particular, inflammatory polyps were only found in the distal colon. The histological distribution of all polyps and cancers found in Group B (patients with only polyps or cancer), in Group C (patients with both diverticula and polyps or cancers), and Group B + Group C is shown in Figure 2; the most frequent histological finding was adenomatous polyps, accounting for 60% (n = 224) of all lesions.
Out of all the 555 patients (Group A + Group B + Group C), 6.7% (37) of them showed a CRC; out of these, 45.9% (17) also showed diverticula. Adenomatous polyps were found in 40.4% (224/555) patients; out of these, 104 (45.4%) also showed diverticula. Hyperplastic polyps were found in 17.5% (97/555) patients; out of these, 38.1% (37) also showed diverticula. Inflammatory polyps were found in 2.5% (14/555) patients; out of these, 71.4% (10) also showed diverticula.
The RR of the association of polyps and cancer with diverticula was assessed. A significant increase in RR of the association of polyps and cancer with diverticula of the colon was found. The RR was higher when only adenomas and cancer were evaluated compared to all types of polyps and cancer (2.81 vs. 2.67, respectively) (Table 3 and Table 4).
At multivariate analysis (Table 5), of the demographic (age, sex) and clinical parameters (family history of colonic diverticula and neoplastic lesions) considered, only diverticula resulted to be significantly associated with colorectal adenomas and cancer (odds ratio (OR) 3.86, 95% CI 2.90–5.14, p < 0.0001).

4. Discussion

Colon cancer could be associated with a history of diverticular disease and personal history of polyps that may be detected during colonoscopy, especially in older patients (>50 years old).
Many studies have been conducted on colonic diverticula but they are heterogeneous due to the different study designs (prospective, retrospective, case-control), the different classes of patients considered (population-based, hospital-admitted, outpatients, etc.), the various methods employed for the diagnosis of diverticula (barium enema, computed tomography (CT), surgery, endoscopy), and the different diseases for which the evaluations were conducted (diverticular disease, diverticulitis, polyps, adenoma, cancer) (Table 6) [1,26,27,28,29,30,31,32,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70].
Most of the evidence available in literature derives from retrospective studies. However, large prospective cohorts have been recently described in Asia [42,49,53,60,65]. Excluding data published in the form of an abstract, to our knowledge, only three prospective studies have been carried out in Caucasian patients [1,26,64] and two in mixed cohorts from the USA [32,41] (Table 6). The incidence and distribution of diverticula in the colon is different between Western countries and Asian countries. In the former, the diverticula are more frequent and develop more in the left colon, while in the latter they predominate in the right colon [2,3,4,5].
In this prospective study, including all consecutive Caucasian patients, we found a significant association of colonic diverticula with colorectal adenomas or cancer. Additionally, the majority of all polyps (including both inflammatory and adenomatous polyps) were found in the distal colon, where diverticula were also more frequently present.
A recent meta-analysis involving 29 cross-sectional studies reported that diverticula were associated with increased risk of adenomas (OR 1.47, 95% CI 1.18–1.84) and with the more lax-defined “polyps” (OR 1.95, 95% CI 1.15–3.31), but not with CRC (OR 0.98, 95% CI 0.63–1.50) [71], as reported in an old case-control study [36]. Interestingly, a sub-analysis showed that diverticulosis did not increase the risk of adenomas (OR 1.34, 95% CI 0.87–2.06) in patients who underwent screening colonoscopy [71]. The latter result might be related by the younger age of patients undergoing their first endoscopic CRC-screening. However, this work shows some limitations, such as the inclusion of cross-sectional studies (in which the causal relationship is difficult to assess), studies in which polyps were defined morphologically regardless of histologic evaluation, and the inclusions of data reported only in the form of abstracts.
In contrast with the results of the aforementioned meta-analysis [71], a cross-sectional study involving 2310 patients by Rondagh et al. reported that the association of diverticulosis with colorectal polyps was influenced by patient age: only below the age of 60 was the prevalence of colorectal polyps significantly higher in patients with diverticulosis than in those without diverticulosis [1]. An association with the female gender has also been described [41].
In the present study, all subtypes of polyps have been considered. The majority of all polyps were found in the distal colon. In particular, inflammatory polyps were only found in the distal colon. Adenomas accounted for 60% of all polyps. A significant increase in relative risk (RR 2.81, 95% CI 2.27–3.47, p < 0.0001) of colorectal adenoma and cancer in patients with colonic diverticula was found. At multivariate analysis, of the demographic and clinical parameters considered, only diverticula resulted in a significant association with colorectal adenomas and cancer (OR 3.86, 95% CI 2.90–5.14, p < 0.0001).
The location of inflammatory polyps in the distal colon confirms literature data, probably due to the presence of a mucosal inflammation of this colonic tract more commonly involved by diverticula [25,72,73,74,75]. Inflammatory polyps develop as a result of an exuberant mucosal regeneration and repair of mucosal inflammatory lesions. The inflammatory polyps are found not only in IBD but also in infectious colitis, ischemic colitis, necrotizing enterocolitis, graft versus host disease, and colonic anastomosis. In non-IBD colitis, inflammatory polyps do not represent a risk factor for CRC.
The association between colonic diverticula and colorectal adenomas and cancer could be related to the epithelial proliferation of colonic mucosa. An upward shifting of cellular proliferation in the colonic mucosa of patients with diverticula was demonstrated and compared with age-matched controls. The cell proliferation index in patients with asymptomatic diverticulosis is three-fold higher than that of healthy controls [76]. It is not clear whether this abnormal epithelial proliferation in colonic diverticula could be responsible for the development of inflammatory polyps, as well as colorectal adenomas and CRC.
In the cohort of patients considered in this study, differences in the frequency of polyps and cancer in patients with diverticulosis, SUDD, SCAD, and diverticulitis have not been detected.
Pathophysiology of diverticulosis is multifactorial, involving genetic predisposition, thickening of the circular and longitudinal muscle wall, elastosis, weakening of the colonic wall, altered neuromuscular activity, environmental factors, age, alteration of microbiota, and inflammation [77,78]. Environmental factors, age, microbiota, and inflammation are also implicated in the pathogenesis of colorectal carcinogenesis [24,79,80,81,82,83].
It has been reported that patients with DD, but also patients with asymptomatic diverticulosis, may display microscopic or macroscopic mucosal signs of mucosal inflammation [25,72]. The relation between chronic inflammation and cancer is well known. Patients with IBD have a significantly higher risk of developing CRC than unaffected subjects, a risk that increases with the extension and duration of the disease [82,83,84]. Furthermore, the epithelial hyper-proliferation of colon crypts, observed both in DD and asymptomatic diverticulosis [85], could be a potential cellular mechanism, leading to a possible increased risk of developing adenomas and CRC in patients with colonic diverticula. It is important to assess whether this increased risk of colorectal adenomas and cancer is linkable to colonic diverticula in general or only to chronic diverticulitis or diverticula with specific genetic and epigenetic variants.
On the other hand, some studies have hypothesized a protective effect of diverticula on CRC development [44]. It should also be noted that not all forms of chronic inflammation of the colon are associated with an increased risk of CRC. Recently, it was reported that microscopic colitis, chronic colitis with the same incidence and prevalence as IBD, appeared to show a reduced risk of adenomas and CRC [86,87].
However, our study shows, some limitations. As this was a cross-sectional study, it was not possible to establish the causal relationship between DD and neoplasm, as well as the future risk of developing CRC in patients with diverticulosis.
Moreover, the indication of a surveillance colonoscopy for a history of polyps was largely self-reported by the patient. Similarly, familial history of CRC and colonic diverticula were also self-reported by patients.
An additional possible limitation is represented by the non-systematic use of validated scales, reporting the extent of diverticulosis and inflammation, or the Paris classification, as the aim of the study focused on histologic findings.
Finally, results involving patients with cancer may be hampered by the limited number of CRCs detected in our study.
However, with the aforementioned limitations, the importance of our study derives not only from being a prospective study including a homogenous population of Caucasian patients but also from a detailed endoscopic localization of diverticula, polyps, and cancers in the various tracts of the large bowel and a histological definition of the various types of polyps and cancer detected.

5. Conclusions

Diverticula and adenomas are frequently found during colonoscopies in adult and elderly patients; however, the evidence of the association between these two conditions is still conflicting.
In our cohort of Caucasic patients, colonic diverticula and colorectal polyps resulted in a significant association, more so for colorectal adenomas and cancer. This finding suggests that patients with colonic diverticula, harboring a higher risk for dysplastic lesions, could require more vigilant endoscopic surveillance than the general population.
However, the present study was not designed to assess follow-up risk. Thus, further prospective large-scale population studies with a long follow-up are needed to corroborate the evidence supporting the relationship between colonic diverticula and colorectal adenomas and CRC, as well as to determine the best time interval between endoscopic examinations.

Author Contributions

Conceptualization, G.L.; design, G.L.; Supervision, G.L. and A.V.; data curation, A.V., F.C., F.V., D.G., G.V., G.S., and A.C.; data analysis and interpretation, S.N., A.V., H.A., and G.L.; writing, A.V. and G.L. All authors have read and agreed to the published version of the manuscript.

Funding

No financial support was received for this study.

Institutional Review Board Statement

The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Institutional Review Board of the University of L’Aquila, 67100 L’Aquila, Italy (Protocol Number: 43958).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

No additional data are available.

Conflicts of Interest

The authors declare no conflict of interest.

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Medicina 57 00108 g001 550
Figure 1. Study population.
Figure 1. Study population.
Medicina 57 00108 g001
Medicina 57 00108 g002 550
Figure 2. Histological distribution of all polyps and cancers found in Group B (patients with only polyps or cancer), in Group C (patients with both diverticula and polyps or cancers), and Group B + Group C.
Figure 2. Histological distribution of all polyps and cancers found in Group B (patients with only polyps or cancer), in Group C (patients with both diverticula and polyps or cancers), and Group B + Group C.
Medicina 57 00108 g002
Table
Table 1. Demographic and clinical characteristics.
Table 1. Demographic and clinical characteristics.
GROUP AGROUP BGROUP CGROUP D
DiverticulaPolyps or CancerPolyps or Cancer and DiverticulaNo Diverticula, Polyps, or Cancer
(N.183)(N.204)(N.168)(N.935)
Age (Years)
Median (Range)68 (27–92)63 (21–93)68 (47–92)65 (29–90)
Sex
Female N (%)88 (48%)95 (47%)64 (38%)410 (44%)
Male N (%)95 (52%)109 (53%)104 (62%)525 (56%)
Family history of CRC
Negative N (%)166 (90.71%)152 (74.51%)143 (85.12%)783 (83.74%)
Positive N (%)17 (9.29%)52 (25.49%)25 (14.88%)152 (16.26%)
Family history of DD
Negative N (%)178 (97.27%)202 (99.02)160 (95.24%)910 (97.33%)
Positive N (%)5 (2.73%)2 (0.98)8 (4.76%)25 (2.67%)
Colorectal cancer (CRC); diverticular disease (DD).
Table
Table 2. Histological characteristics and localization of colorectal polyps and cancer in patients with diverticula of the colon (Group C).
Table 2. Histological characteristics and localization of colorectal polyps and cancer in patients with diverticula of the colon (Group C).
Localization of Diverticula in the Colon TractsHistology
Inflammatory
Polyps
N (%)
10 (6.0%)		Hyperplastic Polyps
N (%)
37 (22.0%)		Adenomas
N (%)
104 (61.9%)		Cancer
N (%)
17 (10.1%)
Proximal colon02 (5.4%)2 (1.9%)2 (11.8%)
Distal colon10 (100%)29 (78.4%)70 (67.3%)15 (88.2%)
Proximal and distal colon0 6 (16.2%)32 (30.8%)0
Table
Table 3. The relative risk of the association of colorectal polyps and cancer with diverticula of the colon.
Table 3. The relative risk of the association of colorectal polyps and cancer with diverticula of the colon.
Polyps and CancersDiverticulaTotal
AbsentPresent
Absent9351831118 (75.0%)
Present204168372 (25.0%)
Total11393511490
Relative risk
2.67
95% CI
2.27 to 3.15
Significance level
p < 0.0001
Table
Table 4. Relative risk of the association of colorectal adenoma and cancer with diverticula of the colon.
Table 4. Relative risk of the association of colorectal adenoma and cancer with diverticula of the colon.
Adenoma and CancersDiverticulaTotal
AbsentPresent
Absent9992301229 (82.5%)
Present140121261 (17.5%)
Total11393511490
Relative risk
2.81
95% CI
2.27 to 3.47
Significance level
p < 0.0001
Table
Table 5. Multivariate analysis with logistic regression and adjusted odds ratios (OR). Multiple logistic regression analyses including age, sex, family history for CRC, family history for diverticula, and presence of diverticula were carried out to investigate the independent association with colorectal polyps.
Table 5. Multivariate analysis with logistic regression and adjusted odds ratios (OR). Multiple logistic regression analyses including age, sex, family history for CRC, family history for diverticula, and presence of diverticula were carried out to investigate the independent association with colorectal polyps.
VariablesOdds Ratiop Value
(95% CI)
Age
per year1.00 (0.99–1.01)0.753
Sex
female1 (reference)0.836
male0.97 (0.74–1.28)
Family history of CRC
No1 (reference)0.162
Yes 1.32 (0.90–1.94)
Family history of DD
No1 (reference)0.467
Yes0.71 (0.28–1.78)
Diverticula
No1 (reference)<0.0001
Yes3.86 (2.90–5.14)
Table
Table 6. Studies evaluating the association between colonic diverticula and colorectal neoplasia.
Table 6. Studies evaluating the association between colonic diverticula and colorectal neoplasia.
StudyStudy DesignN. PatientsMean AgeOutcomes AssessedDiagnosisAssociation
McCallum A
1988 [35]		Retrospective119--Association between diverticulosis and CRCBarium enemano
Morini S
1988 [36]		Case-control study15057.0Association between diverticular disease, adenomas, and CRCColonoscopyYes for adenomas
No for CRC
Stefansson T
1993 [37]		Retrospective7159--Association between diverticulosis or diverticulitis and CRCNationwide registerTwo-fold
increase in the RR of left-sided CRC in patients with diverticulosis or diverticulitis.
Yusuf MA
2000 [38] a		Retrospective31145.3Association between diverticular disease and CRCColonoscopyno
Loffeld R.J
2002 [39]		Retrospective908652.0 without DD
69.0 with DD		Association between diverticulosis and CRC or polyps
(histological type unspecified)		ColonoscopyNo for CRC
yes for polyps
Morini S
2002 [26]		Prospective63066.8 with DD
61.5 without DD		Association between diverticular disease, adenomas, and CRCColonoscopyYes for adenomas
No for CRC
Stefansson T
2004 [40]		Retrospective7159--Association between sigmoid diverticulitis and increased risk of left-side CRCBarium enemayes
Kieff BJ
2004 [41]		Prospective50258.6Association between diverticulosis and CRCColonoscopy CT scan surgery barium enemaYes, only for women with extensive distal diverticulosis
Rajendra S
2005 [42]		Prospective41051.7Association between diverticular disease and adenomasColonoscopyyes
Soran A
2006 [43]		Retrospective156167.0 with DD
and CRC
61.0 only with DD		Association between diverticulosis and CRCSurgeryno
Krones CJ
2006 [44]		Retrospective132664.0Association between diverticulosis or diverticulitis and CRCSurgeryno
Choi CS
2007 [45]		Retrospective237750.8Association between diverticulosis and CRCColonoscopyyes
Rangnekar AS
2007 [46] a		Prospective308-- Association of diverticulosis and polyps Colonoscopyyes
Hirata T
2008 [47]		Retrospective67258.0Association between diverticular disease and colonic polypsColonoscopyyes
Meurs-Szojda MM 2008 [30]Retrospective424159.0 Association of diverticulosis, diverticulitis, polyps, and CRC Colonoscopyno
Hammoud I
2009 [48] a		Retrospective1668-- Association of diverticulosis and polyps Colonoscopyno
Lee KM
2010 [49]		Prospective103052.2 Association of diverticulosis and polyps Colonoscopyyes
Mazumder MK
2011 [50] a		Retrospective100057.3 Association of diverticulosis and polyps Colonoscopyyes
Neubauer K
2011 [51] a		Retrospective177652.5Association between diverticulosis and colorectal adenomas and CRCColonoscopyYes for adenomas
No for CRC
Rondagh EJ
2011 [1]		Prospective231058.4Association between diverticulosis and colorectal polyps (adenoma, serrated polyp, advanced CRC)Colonoscopyyes
Grandlund J
2011 [31]		Retrospective41,03775.0 F
73.0 M		Association between diverticular disease and CRCCT-scan Colonoscopyno
Szura M
2011 [52] a		Retrospective22,44155.1 Association of diverticulosis and polyps Colonoscopyyes
Gohil VB
2012 [28]		Retrospective30057.0Association between diverticulosis and adenoma detection rateColonoscopyyes
Lee SJ
2012 [53]		Prospective60456.9 Association of diverticulosis and CRC CT-colonographyno
Azzam N
2013 [54]		Retrospective27060.82Association among colonic polyps, comorbidities, and diverticular diseaseColonoscopyYes for diverticulosis and adenomas
Parava P
2013 [55] a		Retrospective107757.0 Association of diverticulosis and polyps Colonoscopyyes
Muhammad A
2014 [29]		Retrospective222363.0 with DD
59.0 without DD		 Association between diverticulosis and colorectal polyps (adenomas and advanced adenomas) ColonoscopyYes for adenomas
Lecleire S
2014 [56]		Retrospective40460.9 with DD
60.7 without DD		 Association between acute diverticulitis and colorectal polyps Colonoscopyno
Meda S
2014 [57] a		Retrospective890-- Association of diverticulosis and polyps Colonoscopyno
Shen H
2014 [58] a		Prospective136359.3 Association of diverticulosis and adenomas Colonoscopyno
Huang WY
2014 [59]		Retrospective41,35956.0Association between diverticulosis or diverticulitis and CRCColonoscopyno
Ashktorab H
2015 [27]		Retrospective198657.0Association between diverticulosis and pre-neoplastic colonic lesions (hyperplastic polyps and adenomas)Colonoscopyyes
Peery AF
2015 [32]		Prospective62456.0 with adenoma
53.0 without		Association between colonic diverticula and adenomas or advanced adenomasColonoscopyno
Wang FW
2015 [60]		Prospective189952.8 Association of diverticulosis and adenomas Colonoscopyyes
Wong ER
2016 [61]		Retrospective276653.2Association between colonic diverticula and CRC or polyps (not specified the histological type)Colonoscopyyes
Levine I
2017 [62]		Retrospective58963 with D
58 without D		Association between colonic diverticula and CRC or polypsColonoscopyno
Shah R
2017 [63] a		Retrospective896-- Association of diverticulosis and polyps Colonoscopyyes
Teixeira C
2017 [64]		Prospective20365.5 Association of diverticulosis and adenomas Colonoscopyno
Hong W
2018 [65]		Prospective17,45653.5 with D
49 without D		Association of diverticulosis or location of diverticulosis and adenoma or advanced adenomaColonoscopyno
Pavão Borges V 2018 [66] aRetrospective41467.2 Association of diverticulosis and adenomas Colonoscopyno
Rodriguez-Castro K 2018 [67] aProspective25,96267.2 with D
58.1 without D		Association between colonic diverticula and CRC or polypsColonoscopyYes for adenomas
No for CRC
Schramm C
2018 [68]		Retrospective419665.6 with D
62.0 without D		Association between colonic diverticula and CRC or polypsColonoscopyYes for adenomas
No for CRC
Wang SF
2019 [69]		Retrospective346,11856Association between colonic diverticula and CRC or polypsColonoscopyyes
Tomaoglu K
2020 [70]		Retrospective349651.3 M
53.3 F		Association between diverticulosis and CRC or polypsColonoscopyYes for adenomas
No for CRC
CRC = Colorectal Cancer; DD = Diverticular Disease; RR = Relative Risk; CT = Computed Tomography; a = Data published only in Abstracts.
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Viscido, A.; Ciccone, F.; Vernia, F.; Gabrieli, D.; Capannolo, A.; Stefanelli, G.; Necozione, S.; Valerii, G.; Ashktorab, H.; Latella, G. Association of Colonic Diverticula with Colorectal Adenomas and Cancer. Medicina 2021, 57, 108. https://doi.org/10.3390/medicina57020108

AMA Style

Viscido A, Ciccone F, Vernia F, Gabrieli D, Capannolo A, Stefanelli G, Necozione S, Valerii G, Ashktorab H, Latella G. Association of Colonic Diverticula with Colorectal Adenomas and Cancer. Medicina. 2021; 57(2):108. https://doi.org/10.3390/medicina57020108

Chicago/Turabian Style

Viscido, Angelo, Fabiana Ciccone, Filippo Vernia, Dolores Gabrieli, Annalisa Capannolo, Gianpiero Stefanelli, Stefano Necozione, Giorgio Valerii, Hassan Ashktorab, and Giovanni Latella. 2021. "Association of Colonic Diverticula with Colorectal Adenomas and Cancer" Medicina 57, no. 2: 108. https://doi.org/10.3390/medicina57020108

APA Style

Viscido, A., Ciccone, F., Vernia, F., Gabrieli, D., Capannolo, A., Stefanelli, G., Necozione, S., Valerii, G., Ashktorab, H., & Latella, G. (2021). Association of Colonic Diverticula with Colorectal Adenomas and Cancer. Medicina, 57(2), 108. https://doi.org/10.3390/medicina57020108

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