Abstract
Background and Aims
Recent increases in colorectal cancer (CRC) incidence in adults less than 50 years of age have led to more colonoscopies in this age group. As a result, there may be an increasing number of adults <50 with polyps detected. There is concern that younger adults may require closer follow-up. Our goal was to use data from the New Hampshire Colonoscopy Registry (NHCR) to examine the risk for metachronous advanced adenomas and large (>1cm) serrated polyps in younger versus older adults who return for a follow-up colonoscopy.
Methods
Our cohort consisted of NHCR participants with at least one polyp on index examination and a follow-up colonoscopy at least 1 year after the index examination. Outcomes were the risks for metachronous advanced adenomas (AA: adenomas ≥1cm, with villous elements or high-grade dysplasia, or CRC) and large (≥1 cm) serrated polyps (SP). We present absolute risk and adjusted risks from a logistic regression model stratified by age at index colonoscopy (<40, 40-49, 50-59, and 60+ [ref]). Covariates included index findings, endoscopist adenoma detection rates, sex, smoking, body mass index (BMI), follow-up time (months), bowel preparation quality, and family history of CRC.
Results
In our sample of 12,380 adults, absolute risk for metachronous AA was lower for younger patients than for patients ≥age 60. After adjusting for covariates, when comparing to the 60+ group (reference), the lowest risk was observed in those < 40 (OR, 0.19; 95% CI, 0.05-0.80). Of note, similar risks were observed in the 40 to 49 (OR, 0.61; 95% CI, 0.41-0.92) and 50 to 59 (OR, 0.71; 95% CI, 0.58-0.86) groups. The risk for large metachronous SPs was not associated with age.
Conclusions
Younger adults <40 with index adenomas had a lower risk for metachronous AAs than those ≥60. The 40- to 49-year age group was found to have metachronous risk similar to the 50- to 59-year age group, with both less than the ≥60 age group. These data suggest that current surveillance interval guidelines for patients ≥50 may appropriately be used with younger adults.
Background
Colorectal cancer (CRC) is the second most common cause of death from cancer in the United States, despite being preventable through screening and surveillance. The key to prevention and early detection is screening and appropriate endoscopic follow-up in those adults with polyps. Thus, evidence to support optimal practice, including appropriate intervals at which to repeat the colonoscopies, is critical to inform best practice. One area in need of additional evidence concerns appropriate surveillance intervals for younger adults who are diagnosed with adenomas. A recent study showed that endoscopists may recommend shorter surveillance intervals for younger adults with colorectal neoplasia1. An accompanying editorial highlighted the need for more data regarding the risk of metachronous advanced adenomas in younger adults undergoing surveillance colonoscopies2 This issue may become more pressing due to the anticipated increase in colonoscopies performed on younger individuals as a result of increasing awareness of the colorectal cancer burden in younger adults3-6. Recent data show that there has already been an increase in the number of colonoscopies performed in the 45- to 49-year age group, even before the American Cancer Society’s recommendation to start screening at 45 years6, 7. As a result of the increased number of colonoscopies being performed, more younger adults will likely be diagnosed with adenomas and serrated polyps.
Recommendations for surveillance intervals such as those from the United States Multi-Society Taskforce for Colorectal Cancer Screening are intended for those over 50 years8. It is not clear if these guidelines are appropriate for younger adults with adenomas. It is possible that in individuals who develop adenomas at a younger age, the subsequent adenomas might develop more quickly. Conversely, because increasing age is a strong risk factor for colorectal neoplasia, younger patients may have a lower risk for future lesions. If that were the case, it would seem that currently recommended intervals would provide adequate protection from CRC in younger adults. Therefore, more data are needed to guide surveillance of conventional adenomas in younger adults. In addition, little data exist assessing the metachronous risk of large (≥1 cm) serrated polyps, even for those over 50 years9.
Some previous studies have shown that younger adults might be at lower risk for metachronous adenomas. Most of these studies have been conducted in Asian populations10 or limited by sample size, which precluded definite conclusions about risk for metachronous advanced adenomas11, 12. The New Hampshire Colonoscopy Registry (NHCR), described in detail elsewhere, was founded in 2004 as a population-based, statewide registry collecting data from endoscopy sites throughout New Hampshire (NH) 13-15. The NHCR collects comprehensive index and follow-up data in the longitudinal database. Our goal was to use data from the NHCR to examine the risk for metachronous advanced adenomas and large serrated polyps in younger versus older adults undergoing follow-up colonoscopy.
Methods
Population
Our cohort was selected from the NHCR. Before colonoscopy, consenting patients complete a self-administered Patient Questionnaire which collects data on demographic factors (eg, age, sex, weight), health behaviors (eg, smoking, aspirin use and exercise), and detailed family and personal history of polyps and CRC. Endoscopists or their endoscopy nurses complete the NHCR colonoscopy procedure form immediately after the examination has been completed. Data collected include detailed indication for the examination, findings and quality of bowel preparation.
The NHCR requests pathology reports for all colonoscopies with findings directly from the pathology laboratory used by each participating endoscopy facility. Trained NHCR staff abstract and enter these pathology findings into the NHCR database, including location, size, and histology of each polyp, matching individual polyp level pathology data to information from the colonoscopy Procedure Form.15 All data collection and study procedures were approved by the Committee for the Protection of Human Subjects at Dartmouth College (study no. 00015834), as well as by other relevant human subjects reviewing bodies at participating sites.
Cohort
We included data from individuals with a polyp detected at index examination and a surveillance examination performed at least 12 months after the index. Examinations that were incomplete or had poor bowel preparation and individuals with familial syndromes or inflammatory bowel disease were not included in the cohort.
Exposure variable
Individuals were divided into 4 groups based on age: <40, 40 to 49, 50 to 59, and 60+ years. These groups were chosen to further stratify the younger age group (<50 years) and to provide an older comparison group (60+) to further examine the association of age on risk for metachronous adenomas.
Covariates
The covariates examined were patient, sex, body mass index (BMI), family history of CRC (defined as at least one first-degree relative with CRC), diagnostic indications, index findings (1-2 small [< 1 cm] tubular adenomas, advanced adenomas, 3 or more adenomas and CSSP), smoking (never, past, and current), previous colorectal neoplasia (surveillance indication), aspirin use (none versus once per week) and exercise (never versus at least once per week). Because many index colonoscopies in younger adults are performed for diagnostic purposes, we examined these indications by dividing the symptoms into 2 groups; those that may be clinically insignificant (such as abdominal pain and constipation) versus bleeding symptoms (including iron deficiency anemia and occult bleeding), which may be more significant as suggested by a previous study16. All variables were considered categorical except for age, BMI, endoscopist ADR (number of screening examinations with adenomas divided by total number of screening examinations for each endoscopist), and months since the index examination, which were continuous variables. Index findings were categorized by advanced adenomas, 3 or more adenomas, any 1 to 2 nonadvanced (small tubular) adenomas and clinically significant serrated polyp (CSSP). AAs were defined as adenomas ≥1cm or those with villous elements, high-grade dysplasia, or CRC. CSSP were defined as any sessile serrated adenoma/polyp (SSA/P), traditional serrated adenoma (TSA), and any hyperplastic polyp ≥1 cm anywhere in the colon or any hyperplastic polyp >5 mm in the proximal (proximal to sigmoid) colon only.
Statistical approach
Outcomes were the absolute and adjusted risk of AAs or large (≥1 cm) serrated polyps presented in the 4 age categories outlined above. For the descriptive statistics, we used the chi square test for trend and the Fisher exact test to evaluate categorical variables. Wilcoxon rank sum and Mann-Whitney tests were used for nonparametric continuous variables. We performed univariate analyses and multivariable logistic regression models comparing predictors of advanced adenomas, any adenomas and CSSP. Covariates in the multivariable analysis included age (continuous), sex, BMI (continuous), ADR (continuous) of index and surveillance endoscopist, family history of CRC, surveillance indication (previous colorectal neoplasia), diagnostic indications, aspirin use, index findings (1-2 small [< 1 cm] tubular adenomas, advanced adenomas, 3 or more adenomas and CSSP), smoking (never, past or current) and exercise.
Results
There were 12,380 individuals who met the inclusion criteria and were stratified by index findings into the 4 age groups as per the categories outlined above; 266 in the <40 group, 1063 in the 40 to 49 groups, 5238 in the 50 to 59 group and 5813 in the 60+ group. Characteristics for these groups, including age, sex, BMI, and lifestyle factors, are shown in Table 1. The mean time to follow-up for each age group was: 48.5 months (± 28.3 SD) for those <40, 55.1 (± 27.9) months for those 40 to 49, 57.0 (± 26.3) for those 50 to 59, and 51.0 (± 22.6) months for those 60 years and older. The prevalence of diagnostic indications for the index examinations, as divided into clinically insignificant symptoms (eg, abdominal pain) and bleeding symptoms are shown in Table 1.
Table 1.
Demographics and examination characteristics for analyzed sample (n=12,380) as stratified by age group.
| <40 (n=266) |
40-49 (n=1063) |
50-59 (n=5238) |
60+ (n=5813) |
||
|---|---|---|---|---|---|
| Age (years) (avg ± SD) | 33.5±5.1 | 45.5±2.7 | 54.0±3.0 | 67.0±5.4 | |
| Sex (M) | 39.1% (104) |
48.5% (515) |
53.9% (2823) |
57.6% (3345) |
|
| BMI (continuous) (avg ± SD) | 28.6±7.0 | 29.1±6.4 | 29.0±6.1 | 28.6±5.7 | |
| Race (% white) | 87.6% (233) |
91.0% (967) |
93.0% (4870) |
93.8% (5452) |
|
| Family history (first-degree relative) | 23.7% (63) |
35.7% (379) |
20.4% (1069) |
24.9% (1446) |
|
| Advanced* adenomas on index examination | 7.1% (19) |
11.1% (118) |
12.6% (658) |
13.8% (803) |
|
| 3 or more adenomas on index examination | 1.5% (4) |
4.2% (45) |
6.2% (325) |
10.9% (631) |
|
| High-risk adenomas on index | 8.6% (23) |
15.3% (163) |
18.8% (983) |
24.7% (1434) |
|
| 1-2 small tubular adenomas on index | 41.3% (78) |
40.0% (338) |
48.5% (2039) |
47.8% (2261) |
|
| CSSP on index examination** | 10.5% (28) |
12.7% (135) |
13.1% (687) |
11.9% (690) |
|
| Surveillance examination | 12.4% (33) |
18.3% (194) |
21.3% (1118) |
43.3% (2516) |
|
| Bleeding symptoms | 21.4% (57) |
19.7% (209) |
4.2% (218) |
4.9% (287) |
|
| Clinically insignificant symptoms | 39.5.7% (105) |
22.2% (237) |
4.4% (233) |
5.4% (315) |
|
| Fair bowel preparation | 9.8% (26) |
10.9% (116) |
9.7% (509) |
10.8% (627) |
|
| Smoking | Never | 43.9% (111) |
51.5% (529) |
47.0% (2375) |
39.9% (2243) |
| Past | 30.8% (78) |
29.5% (299) |
38.0% (1922) |
52.1% (2923) |
|
| Current | 25.3% (64) |
19.3% (200) |
15.0% (758) |
8.0% (449) |
|
| Aspirin (1 time/week) | 12.4% (30) |
19.7% (195) |
33.1% (1604) |
55.7% (2993) |
|
| Exercise (1/week or more) | 48.2% (121) |
51.2% (522) |
55.8% (2820) |
54.0% (3021) |
|
| Time to follow-up examination (months) (avg ± SD) | 48.5±28.3 | 55.1±28.0 | 57.0±26.3 | 51.0±22.6 | |
Advanced adenomas: ≥1cm or those with villous elements, high-grade dysplasia, or CRC
CSSP: SSA/P, TSA, and any HP >1 cm or any HP >5 mm in the proximal (proximal to sigmoid) colon only.
The absolute risk for metachronous advanced adenomas and large (≥1 cm) serrated polyps are shown in Table 2 and Figure 1. The absolute risk for metachronous AA was significantly less in younger adults than in the ≥60 age group. The absolute risk for metachronous CRC in younger adults was lower than that for older adults; <40 years (0.0%; 0/266), 40 to 49 years (0.2%; 2/1063); 50 to 59 (0.2%; 9/5238), and 60+ years (0.4%; 26/5813) (p=0.04). With regard to the diagnostic symptoms, neither was associated with an increased risk for metachronous advanced adenomas. Specifically, there was no statistically significant difference between those with bleeding symptoms (44/771; 5.7%) versus those without (657/11609; 5.7%) (p=1.0) and those with (39/890; 4.4%) or without nonbleeding symptoms (662/11490; 5.8%) (p=0.10). Older age effect was less pronounced in CSSPs.
Table 2.
Risks and ORs for metachronous advanced adenomas and large serrated polyps across age groups
| Metachronous advanced adenomas | Metachronous large serrated polyp | |||||
|---|---|---|---|---|---|---|
| Age group |
Absolute risk |
Unadjusted OR (95% CI) |
Adjusted OR (95% CI) |
Absolute risk |
Unadjusted OR (95% CI) |
Adjusted OR (95% CI) |
| < 40 (n=266) |
0.8% (n=2) |
0.10 (0.02-0.39) |
0.19 (0.05-0.80) |
1.1% (n=3) |
0.47 (0.15-1.48) |
0.38 (0.1-1.29) |
| 40-49 (n=1063) |
3.7% (n=39) |
0.49 (0.35-0.68) |
0.61 (0.41-0.92) |
2.7% (n=29) |
1.15 (0.77-1.73) |
1.12 (0.69-1.83) |
| 50-59 (n=5238) |
4.5% (n=237) |
0.60 (0.51-0.71) |
0.71 (0.58-0.86) |
2.8% (n=146) |
1.18 (0.93-1.49) |
1.02 (0.76-1.38) |
| 60+ (n=5813) |
7.3% (n=423) |
1.0 (reference) |
1.0 (reference) |
2.4% (n=138) |
1.0 (reference) |
1.0 (reference) |
Models adjusted for age, sex, BMI, any family history of CRC, smoking and other covariates listed in Table 3.
Figure 1.
Absolute risk of metachronous advanced adenomas and large serrated polyps across age categories.
After adjusting for covariates, when comparing with the 60+ group (reference), the lowest risk was observed in those <40 (OR, 0.19; 95% CI, 0.05-0.80). Of note, similar risks were observed in the 40 to 49 (OR, 0.61; 95% CI, 0.41-0.92) and 50 to 59 (OR, 0.71; 95% CI, 0.58-0.86) groups. These results are shown in Table 2. After adjustment for co-variates, older age effect, once again, was not associated with risk for metachronous CSSPs. The results for the covariates including examination level (index findings and endoscopist ADR for index and surveillance examination) and patient level, which were included in the models, are shown in Table 3. There was a slight trend for the index endoscopists ADR to be inversely associated with detection of a follow-up advanced adenoma and for a higher ADR for the surveillance endoscopist to be associated with an increase risk in detection of adenomas on surveillance examination.
Table 3.
Baseline patient and examination level characteristics and risk for metachronous advanced adenomas and large serrated polyps (covariates in the logistic model in Table 2)
| Advanced adenoma (OR 95% CI) |
Large serrated polyp (OR 95% CI) |
||
|---|---|---|---|
| Sex (F versus M) | 0.87 (0.72-1.04) | 1.08 (0.82-1.41) | |
| BMI (continuous) | 1.02 (1.01-1.03) | 1.00 (0.98-1.03) | |
| Family history (first-degree relative) | 1.08 (0.87-1.32) | 0.70 (0.50-0.98) | |
| Smoking | Never | 1.0 (ref) | 1.0 (ref) |
| Past | 1.07 (0.88-1.30) | 1.11 (0.82-1.50) | |
| Current | 1.21 (0.91-1.61) | 2.25 (1.56-3.22) | |
| ADR index endoscopist | 0.99 (0.97-1.00) | 0.99 (0.97-1.01) | |
| ADR surveillance endoscopist | 1.01 (1.00-1.03) | 1.05 (1.03-1.07) | |
| Aspirin (1 time/week) | 0.99 (0.82-1.20) | 0.77 (0.58-1.04) | |
| Exercise (1/week or more) | 0.81 (0.68-0.98) | 0.93 (0.71-1.23) | |
| Advanced adenomas on index | 3.99 (2.92-5.44) | 0.56 (0.36-0.89) | |
| 3 or more adenomas on index | 3.22 (2.28-4.55) | 0.52 (0.31-0.89) | |
| Nonadvanced adenoma on index | 1.71 (1.30-2.26) | 0.61 (0.45-0.84) | |
| CSSP on index | 1.30 (1.00-1.70) | 3.26 (2.43-4.36) | |
| Surveillance indication for index | 1.25 (1.03-1.53) | 1.35 (1.10-1.81) | |
| Clinically insignificant symptoms | 1.04 (0.68-1.58) | 1.47 (0.89-2.40) | |
| Bleeding symptoms | 1.19 (0.81-1.74) | 0.44 (0.19-1.02) | |
| Months since index examination | 1.00 (1.00-1.01) | 0.99 (0.99-1.00) | |
To explore the impact of follow-up time on the risk for metachronous adenomas, we restricted our analysis to those adults with a follow-up examination at least 3 years (36 months) after the index and observed no change in our results. In this restricted analysis, the mean time to follow-up for each age group was: 63.0 months (± 25.3 SD) for those <40, 65.2 (± 24.3) months for those 40 to 49, 64.2 (± 22.8) for those 50-59 and 59.0 (± 18.4) months for those 60 years and older. These data are shown in Table 4.
Table 4.
Results of logistic regression model predicting metachronous advanced adenomas as stratified across age groups for those with a follow-up of 36 months or longer
| Absolute risk | Months to follow-up |
Unadjusted OR (95% CI) |
Adjusted OR (95% CI) |
|
|---|---|---|---|---|
| < 40 (n=169) |
1.2% (2) |
63.0±25.3 | 0.16 (0.04-0.64) |
0.18 (0.04-0.75) |
| 40-49 (n=807) |
3.5% (28) |
65.2±24.3 | 0.48 (0.32-0.71) |
0.53 (0.35-0.82) |
| 50-59 (n=4335) |
4.2% (181) |
64.2±22.8 | 0.58 (0.48-0.70) |
0.63 (0.51-0.77) |
| 60+ (n=4553) |
7.0% (320) |
59.0±18.4 | 1.0 (reference) |
1.0 (reference) |
Models adjusted for sex, BMI, index findings, endoscopist ADR, diagnostic and surveillance indications, smoking, aspirin intake, exercise, months to follow-up and previous colorectal neoplasia
To further examine the impact of index findings on the risk for metachronous advanced adenomas, we examined the absolute risk for advanced adenomas, 3 or more adenomas and 1-2 small tubular adenomas (Table 5). The results were similar to the overall results. We also examined the impact of family history of CRC by stratifying the sample into those that had a family history versus those that did not have a family history (Table 6).
Table 5.
Risk for metachronous advanced adenomas across age groups as stratified by index findings.
| Factor | < 40 | 40-49 | 50-59 | 60+ |
|---|---|---|---|---|
| 3 or more adenomas | 25.0% (1/4) |
6.7% (3/45) |
7.4% (24/325) |
10.9% (69/631) |
| Advanced adenomas | 0% (0/19) |
9.3% (11/118) |
8.5% (56/658) |
12.1% (97/803) |
| High-risk adenoma* | 4.3% (1/23) |
8.6% (14/163) |
8.1% (80/983) |
11.6% (166/1434) |
| 1-2 small tubular adenomas** | 1.3% (1/78) |
3.0% (10/338) |
4.3% (88/2039) |
6.0% (135/2261) |
p=0.03
p < 0.001
Table 6.
Risk for metachronous advanced adenomas across age groups as stratified by family history of CRC.
| < 40 | 40-49 | 50-59 | 60+ | ||
|---|---|---|---|---|---|
| Family History CRC (FDR) | Yes | 0% (0/63) |
3.2% (12/379) |
4.8% (51/1069) |
6.8% (98/1446) |
| No | 1.0% (2/203) |
3.9% (27/684) |
4.5% (186/4169) |
7.4% (325/4366) |
Discussion
We observed that younger individuals <50 years of age in our cohort were less likely than older adults > 60 years to have a metachronous advanced adenoma on surveillance colonoscopy. The group with the lowest risk included those individuals who were less than 40 years of age. Of note, similar risks were observed in the 40- to 49-year and 50- to 59-year age groups. Unlike conventional adenomas the risk for metachronous large serrated polyps was not associated with older age.
Our data are important to inform best practice for the surveillance of young adults with adenomas and serrated polyps. A recent study showed that endoscopists frequently recommend surveillance examinations for patients <40 years at intervals earlier than those recommended in the U.S. MSTF guidelines1. Furthermore, in that study, nearly one third of all individuals < 40 years in that study with low risk findings on index colonoscopy were recommended to have a repeat examination within 3 years. These data suggest that endoscopists may be concerned about the potential increased risk for metachronous adenomas in younger adults. Our data showed that younger individuals who had surveillance examinations performed at similar time intervals to older adults had lower risks for metachronous lesions than the older adults. Our results provide a cogent argument that surveillance guidelines for older adults could be used for younger adults. Even in our restricted analysis, where the mean follow-up time (about 5 years) allowed adequate time for adenomas to develop, younger adults had a lower risk for metachronous adenomas.
There have been previous studies which have shown that risk for metachronous advanced adenomas in younger adults is lower than that for older adults10-12, 17, 18. However, some of these studies had relatively small numbers12, 17. In addition, 2 studies have examined only patients who had curative surgery for CRC,17, 19 and therefore these data may not be generalizable to adults without CRC. One recent U.S. study showed that younger adults had a lower risk for metachronous advanced neoplasia than older adults, but this difference was not statistically significant, possibly due to insufficient power11. A recent study from Korea analyzed data from a large sample and observed that younger adults were at lower risk than older adults for future advanced neoplasia10. Some limitations with this study included a short follow-up time of slightly over 3 years even for low-risk adenomas. Another Korean study demonstrated a lower risk for younger adults as compared with individuals >50 years of age18. Although this study included only university centers, our study included data from many different practice types including community and academic. In addition, there were no data in the Korean studies regarding endoscopist quality metrics. Conversely in our study, our follow-up time for all groups was closer to 5 years. Furthermore, we performed a sensitivity analysis examining only those individuals with a follow-up of at least 3 years and observed similar findings. In addition, we included the ADR for the endoscopists performing the index and follow-up colonoscopies in addition to other factors in our logistic regression model and observed that the outcomes were not significantly altered. These data show that a higher endoscopist detection rate in the older groups did not explain the higher risk.
Our study has several additional strengths. We included data from index and repeat colonoscopies performed in over 1300 adults less than 50 years, nearly 300 of whom were less than 40 years of age. This is the largest Western study to date examining the risk of metachronous adenomas and serrated polyps in individuals less than 50 years. Other strengths include the incorporation of several risk factors for conventional and serrated polyps in our analysis such as smoking and BMI9, 20-26. We also stratified our age categories to examine specific age groups, allowing clearer demonstration of the association between age and risk for metachronous adenomas. The youngest group, those less than 40 years of age, were at significantly lower risk than the older group, the 60+ age group. Within our stratified groups, we observed similar risks in the 40- to 49-year and 50- to 59-year age groups. Finally, our study provides data on metachronous large serrated polyps, which have a similar long-term CRC risk as advanced adenomas27. Our data suggest that age did not appear to be a risk factor in this serrated polyp group.
One limitation of our study is that these data are not from controlled trials, thus creating the potential for confounding factors as well as some variability in timing of the examinations. However, we performed a sensitivity analysis examining only those with a follow-up of at least 3 years. In addition, we included many well recognized CRC risk factors in our models, and our data reflect outcomes from “real world” practice. In addition, it should be acknowledged that our study was designed to only examine the risk of metachronous polyps in adults who returned for a repeat colonoscopy and was not designed to investigate any potentially missed interval cancers. Finally, New Hampshire may not have significant racial diversity; however, there is ethnic, socioeconomic and rural/urban diversity in the population seen by practices participating in NHCR28. As always, the results should be confirmed in other settings.
In summary, we observed that younger age was associated with a lower risk for metachronous advanced adenomas than in those older than 60 years. Investigation through our longitudinal database allowed for adequate follow-up time during which new adenomas or serrated polyps could develop. Specifically, we had a mean follow-up time of 4+ years and 5+ years in our main and restricted analyses respectively. During that time period, the risk for metachronous advanced adenomas was lower in the younger population than in the older population. This finding suggests that the intervals recommended in the current surveillance guidelines for older individuals would be appropriate for younger adults with respect to protection from interval advanced lesions.
Acknowledgments
Financial support: The project described was supported by Grant # R01CA131141 and contract # HHSN261201400595P from the National Cancer Institute, as well as by the Norris Cotton Cancer Center. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Cancer Institute or the National Institutes of Health.
Abbreviations and Acronyms
- ADR
Adenoma detection rate
- SSA/P
Sessile serrated adenomas/polyps
- TSA
Traditional serrated adenomas
- HP
Hyperplastic polyps
- AA
Advanced adenoma
- NHCR
New Hampshire Colonoscopy Registry
- ACG
American College of Gastroenterology
- ASGE
American Society for Gastrointestinal Endoscopy
- CRC
Colorectal Cancer
- BMI
Body Mass Index
- IBD
Inflammatory bowel disease
- USMSTF
US Multi Society Task Force
- CSSPs
Clinically significant serrated polyps
- HGD
High grade dysplasia
- HS
High school
Footnotes
The contents of this work do not represent the views of the Department of Veterans Affairs or the United States Government
CONFLICT OF INTEREST: The authors have no conflicts of interest to declare.
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References
- 1.Cha JM, La Selva D, Kozarek RA, et al. Young patients with sporadic colorectal adenomas: current endoscopic surveillance practices and outcomes. Gastrointest Endosc 2018;88:818–825 e1. [DOI] [PubMed] [Google Scholar]
- 2.Cameron K, Moss A. Is 35 the new 50? Challenges in determining colonoscopy surveillance recommendations for young patients with incidentally detected adenomas. Gastrointest Endosc 2018;88:826–829. [DOI] [PubMed] [Google Scholar]
- 3.Ahnen DJ, Wade SW, Jones WF, et al. The increasing incidence of young-onset colorectal cancer: a call to action. Mayo Clin Proc 2014;89:216–24. [DOI] [PubMed] [Google Scholar]
- 4.Patel SG, Ahnen DJ. Colorectal Cancer in the Young. Curr Gastroenterol Rep 2018;20:15. [DOI] [PubMed] [Google Scholar]
- 5.Siegel RL, Miller KD, Jemal A. Colorectal Cancer Mortality Rates in Adults Aged 20 to 54 Years in the United States, 1970–2014. JAMA 2017;318:572–574. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Wolf AMD, Fontham ETH, Church TR, et al. Colorectal cancer screening for average-risk adults: 2018 guideline update from the American Cancer Society. CA Cancer J Clin 2018;68:250–281. [DOI] [PubMed] [Google Scholar]
- 7.Fedewa SA, Siegel RL, Jemal A. Are temporal trends in colonoscopy among young adults concordant with colorectal cancer incidence? J Med Screen 2019:969141319859608. [DOI] [PubMed] [Google Scholar]
- 8.Lieberman DA, Rex DK, Winawer SJ, et al. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2012;143:844–857. [DOI] [PubMed] [Google Scholar]
- 9.Anderson JC, Butterly LF, Robinson CM, et al. Risk of Metachronous High-Risk Adenomas and Large Serrated Polyps in Individuals With Serrated Polyps on Index Colonoscopy: Data From the New Hampshire Colonoscopy Registry. Gastroenterology 2018;154:117–127 e2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Kim NH, Jung YS, Park JH, et al. Risk of developing metachronous advanced colorectal neoplasia after colonoscopic polypectomy in patients aged 30 to 39 and 40 to 49 years. Gastrointest Endosc 2018;88:715–723. [DOI] [PubMed] [Google Scholar]
- 11.Nagpal SJS, Mukhija D, Sanaka M, et al. Metachronous colon polyps in younger versus older adults: a case-control study. Gastrointest Endosc 2018;87:657–665. [DOI] [PubMed] [Google Scholar]
- 12.Park SK, Kim NH, Jung YS, et al. Risk of developing advanced colorectal neoplasia after removing high-risk adenoma detected at index colonoscopy in young patients: A KASID study. J Gastroenterol Hepatol 2016;31:138–44. [DOI] [PubMed] [Google Scholar]
- 13.Weaver DL, Rosenberg RD, Barlow WE, et al. Pathologic findings from the Breast Cancer Surveillance Consortium: population-based outcomes in women undergoing biopsy after screening mammography. Cancer 2006;106:732–42. [DOI] [PubMed] [Google Scholar]
- 14.Butterly LF, Goodrich M, Onega T, et al. Improving the quality of colorectal cancer screening: assessment of familial risk. Dig Dis Sci 2010;55:754–60. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Greene MA, Butterly LF, Goodrich M, et al. Matching colonoscopy and pathology data in population-based registries: development of a novel algorithm and the initial experience of the New Hampshire Colonoscopy Registry. Gastrointest Endosc 2011;74:334–40. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Cha JM, Kozarek RA, La Selva D, et al. Findings of diagnostic colonoscopy in young adults versus findings of screening colonoscopy in patients aged 50 to 54 years: a comparative study stratified by symptom category. Gastrointest Endosc 2015;82:138–45. [DOI] [PubMed] [Google Scholar]
- 17.Kim SB, Lee HJ, Park SJ, et al. Comparison of Colonoscopy Surveillance Outcomes Between Young and Older Colorectal Cancer Patients. J Cancer Prev 2017;22:159–165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Kim HG, Cho YS, Cha JM, et al. Risk of metachronous neoplasia on surveillance colonoscopy in young patients with colorectal neoplasia. Gastrointest Endosc 2018;87:666–673. [DOI] [PubMed] [Google Scholar]
- 19.Tjaden J, Muller C, Wideroff G, et al. Metachronous Advanced Neoplasia on Surveillance Colonoscopy in Young versus Older Onset Colorectal Cancer Patients. Clin Gastroenterol Hepatol 2019. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Anderson JC, Attam R, Alpern Z, et al. Prevalence of colorectal neoplasia in smokers. Am J Gastroenterol 2003;98:2777–83. [DOI] [PubMed] [Google Scholar]
- 21.Anderson JC, Latreille M, Messina C, et al. Smokers as a high-risk group: data from a screening population. J Clin Gastroenterol 2009;43:747–52. [DOI] [PubMed] [Google Scholar]
- 22.Anderson JC, Messina CR, Dakhllalah F, et al. Body mass index: a marker for significant colorectal neoplasia in a screening population. J Clin Gastroenterol 2007;41:285–90. [DOI] [PubMed] [Google Scholar]
- 23.Anderson JC, Moezardalan K, Messina CR, et al. Smoking and the association of advanced colorectal neoplasia in an asymptomatic average risk population: analysis of exposure and anatomical location in men and women. Dig Dis Sci 2011;56:3616–23. [DOI] [PubMed] [Google Scholar]
- 24.Anderson JC, Pleau DC, Rajan TV, et al. Increased frequency of serrated aberrant crypt foci among smokers. Am J Gastroenterol 2010;105:1648–54. [DOI] [PubMed] [Google Scholar]
- 25.Anderson JC, Stein B, Kahi CJ, et al. Association of smoking and flat adenomas: results from an asymptomatic population screened with a high-definition colonoscope. Gastrointest Endosc 2010;71:1234–40. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Anderson JC, Weiss JE, Robinson CM, et al. Adenoma Detection Rates for Screening Colonoscopies in Smokers and Obese Adults: Data From the New Hampshire Colonoscopy Registry. J Clin Gastroenterol 2017;51:e95–e100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Holme O, Bretthauer M, Eide TJ, et al. Long-term risk of colorectal cancer in individuals with serrated polyps. Gut 2015;64:929–36. [DOI] [PubMed] [Google Scholar]
- 28.Rice K, Sharma K, Li C, et al. Cost-effectiveness of a patient navigation intervention to increase colonoscopy screening among low-income adults in New Hampshire. Cancer 2019;125:601–609. [DOI] [PMC free article] [PubMed] [Google Scholar]

