8
ORIGINAL ARTICLE: Clinical Endoscopy Short- and long-term risk of colorectal adenoma recurrence among whites and blacks Adeyinka O. Laiyemo, MD, MPH, 1,2 Chyke Doubeni, MD, MPH, 3 Hassan Brim, PhD, 4 Hassan Ashktorab, PhD, 1 Robert E. Schoen, MD, MPH, 5 Samir Gupta, MD, MSCS, 6 Aline Charabaty, MD, 7 Elaine Lanza, PhD, 8 Duane T. Smoot, MD, 9 Elizabeth Platz, ScD, MPH, 10 Amanda J. Cross, PhD 11 Washington, DC; Bethesda, Maryland; Philadelphia, Pittsburgh, Pennsylvania; Dallas, Texas; Nashville, Tennessee; Baltimore, Maryland, USA Background: It is unclear whether the higher burden from colorectal cancer among blacks is due to an increased biological susceptibility. Objective: To determine whether non-Hispanic blacks (blacks) have a higher risk of adenoma recurrence than non-Hispanic whites (whites) after removal of colorectal adenoma. Design: Secondary analysis of the Polyp Prevention Trial (PPT) data. Setting: United States. Patients: Patients were 1668 self-identified whites and 153 blacks who completed the 4-year trial. Of these, 688 whites and 55 blacks enrolled in a posttrial, passive Polyp Prevention Trial Continued Follow-up Study (PPT-CFS) and underwent another colonoscopy. Main Outcome Measurements: Recurrence and location of the adenoma and advanced adenoma by race- ethnicity during PPT and cumulative recurrence over a mean follow-up of 8.3 years (range, 4.9-12.4 years) among PPT-CFS enrollees. Results: Blacks had similar risk of recurrence of adenoma (39.2% vs 39.4%; incidence risk ratio [RR] .98; 95% CI, .80-1.20) and advanced adenoma (8.5% vs 6.4%; RR 1.18; 95% CI, .68-2.05) as whites at the end of PPT. Recurrence risk did not differ by colon subsite. Among PPT-CFS enrollees, the cumulative recurrence rate over a maximal follow-up period of 12 years was similar for blacks and whites for adenoma (67.3% vs 67.0%; RR 1.01; 95% CI, .84-1.21) and advanced adenoma (14.5% vs 16.9%; RR 1.03; 95% CI, .60-1.79). Limitation: There were few blacks in the long-term follow-up study. Conclusions: Adenoma and advanced adenoma recurrence did not differ by race. Our study does not support more frequent surveillance colonoscopies for blacks with a personal history of adenoma as an intervention to reduce colorectal cancer disparity. ( Gastrointest Endosc 2013;77:447-54.) Abbreviations: blacks, non-Hispanic blacks; CI, confidence intervals; CRC, colorectal cancer; PPT, Polyp Prevention Trial; PPT-CFS, Polyp Prevention Trial Continued Follow-up Study; RR, incidence risk ratio; RRR, relative risk ratio; whites, non-Hispanic whites. DISCLOSURE: Dr Laiyemo is supported by the National Cancer Institute’s new faculty recruitment supplement to the Comprehensive Minority Institution/Cancer Center Partnership between Howard University Can- cer Center and Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins University (5U54CA091431-09 S1). Dr Doubeni is supported by a mentored career development award (5K01CA127118). Dr Platz is supported by National Institutes of Health grant P30 CA006973. The study was funded by the Division of Cancer Prevention and the Intramural Research Program of the Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health. See CME section; p. 491. Copyright © 2013 by the American Society for Gastrointestinal Endoscopy 0016-5107/$36.00 http://dx.doi.org/10.1016/j.gie.2012.11.027 Received September 3, 2012. Accepted November 21, 2012. Current affiliations: Department of Medicine, Howard University Hospital, Washington, DC (1), Division of Cancer Prevention, National Cancer Insti- tute, National Institutes of Health, Bethesda, Maryland (2), Department of Family Medicine and Community Health, University of Pennsylvania Perel- man School of Medicine, Philadelphia, Pennsylvania (3), Department of Pa- thology, Howard University Hospital, Washington, DC (4), Department of Medicine and Epidemiology, University of Pittsburgh, Pittsburgh, Pennsyl- vania (5), Division of Gastroenterology, University of Texas Southwestern (footnotes continued on last page of article) www.giejournal.org Volume 77, No. 3 : 2013 GASTROINTESTINAL ENDOSCOPY 447

Short- and long-term risk of colorectal adenoma recurrence among whites and blacks

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Page 1: Short- and long-term risk of colorectal adenoma recurrence among whites and blacks

ORIGINAL ARTICLE: Clinical Endoscopy

Short- and long-term risk of colorectal adenoma recurrence amongwhites and blacks

Adeyinka O. Laiyemo, MD, MPH,1,2 Chyke Doubeni, MD, MPH,3 Hassan Brim, PhD,4 Hassan Ashktorab, PhD,1

Robert E. Schoen, MD, MPH,5 Samir Gupta, MD, MSCS,6 Aline Charabaty, MD,7 Elaine Lanza, PhD,8

Duane T. Smoot, MD,9 Elizabeth Platz, ScD, MPH,10 Amanda J. Cross, PhD11

Washington, DC; Bethesda, Maryland; Philadelphia, Pittsburgh, Pennsylvania; Dallas, Texas; Nashville, Tennessee;Baltimore, Maryland, USA

Background: It is unclear whether the higher burden from colorectal cancer among blacks is due to an increasedbiological susceptibility.

Objective: To determine whether non-Hispanic blacks (blacks) have a higher risk of adenoma recurrence thannon-Hispanic whites (whites) after removal of colorectal adenoma.

Design: Secondary analysis of the Polyp Prevention Trial (PPT) data.

Setting: United States.

Patients: Patients were 1668 self-identified whites and 153 blacks who completed the 4-year trial. Of these, 688whites and 55 blacks enrolled in a posttrial, passive Polyp Prevention Trial Continued Follow-up Study (PPT-CFS)and underwent another colonoscopy.

Main Outcome Measurements: Recurrence and location of the adenoma and advanced adenoma by race-ethnicity during PPT and cumulative recurrence over a mean follow-up of 8.3 years (range, 4.9-12.4 years) amongPPT-CFS enrollees.

Results: Blacks had similar risk of recurrence of adenoma (39.2% vs 39.4%; incidence risk ratio [RR] � .98; 95%CI, .80-1.20) and advanced adenoma (8.5% vs 6.4%; RR � 1.18; 95% CI, .68-2.05) as whites at the end of PPT.Recurrence risk did not differ by colon subsite. Among PPT-CFS enrollees, the cumulative recurrence rate overa maximal follow-up period of 12 years was similar for blacks and whites for adenoma (67.3% vs 67.0%; RR �1.01; 95% CI, .84-1.21) and advanced adenoma (14.5% vs 16.9%; RR � 1.03; 95% CI, .60-1.79).

Limitation: There were few blacks in the long-term follow-up study.

Conclusions: Adenoma and advanced adenoma recurrence did not differ by race. Our study does not supportmore frequent surveillance colonoscopies for blacks with a personal history of adenoma as an intervention toreduce colorectal cancer disparity. (Gastrointest Endosc 2013;77:447-54.)

Abbreviations: blacks, non-Hispanic blacks; CI, confidence intervals;CRC, colorectal cancer; PPT, Polyp Prevention Trial; PPT-CFS, PolypPrevention Trial Continued Follow-up Study; RR, incidence risk ratio;RRR, relative risk ratio; whites, non-Hispanic whites.

DISCLOSURE: Dr Laiyemo is supported by the National Cancer Institute’snew faculty recruitment supplement to the Comprehensive MinorityInstitution/Cancer Center Partnership between Howard University Can-cer Center and Sidney Kimmel Comprehensive Cancer Center at JohnsHopkins University (5U54CA091431-09 S1). Dr Doubeni is supported bya mentored career development award (5K01CA127118). Dr Platz issupported by National Institutes of Health grant P30 CA006973. Thestudy was funded by the Division of Cancer Prevention and theIntramural Research Program of the Division of Cancer Epidemiologyand Genetics, National Cancer Institute, National Institutes of Health.

See CME section; p. 491.

0016-5107/$36.00http://dx.doi.org/10.1016/j.gie.2012.11.027

Received September 3, 2012. Accepted November 21, 2012.

Current affiliations: Department of Medicine, Howard University Hospital,Washington, DC (1), Division of Cancer Prevention, National Cancer Insti-tute, National Institutes of Health, Bethesda, Maryland (2), Department ofFamily Medicine and Community Health, University of Pennsylvania Perel-man School of Medicine, Philadelphia, Pennsylvania (3), Department of Pa-thology, Howard University Hospital, Washington, DC (4), Department ofMedicine and Epidemiology, University of Pittsburgh, Pittsburgh, Pennsyl-vania (5), Division of Gastroenterology, University of Texas Southwestern

(footnotes continued on last page of article)

Copyright © 2013 by the American Society for Gastrointestinal Endoscopy

www.giejournal.org Volume 77, No. 3 : 2013 GASTROINTESTINAL ENDOSCOPY 447

Page 2: Short- and long-term risk of colorectal adenoma recurrence among whites and blacks

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Race and adenoma recurrence Laiyemo et al

Blacks have the highest incidence of and mortality fromcolorectal cancer (CRC) in the United States.1-3 Studieshave reported that blacks develop CRC at earlier ages withmore right-sided cancers when compared with whites.4,5

They also have more advanced stages of disease whenseeking treatment, even among insured patients when CRCscreening was a covered benefit.6 These factors suggest thatlacks may have a higher biological susceptibility to CRC.owever, there is evidence that black–white differences inRC risk may be related to differences in access to, or use of,ealthcare services.7-11 Furthermore, similar CRC survival was

reported for blacks and whites in the U.S. Veterans AffairsHealth Care System where access to healthcare resources isequivalent12 and also among participants in a randomizedclinical trial of adjuvant chemotherapy.13 These studies sug-est a less important role of biology as the main factor forRC disparity by race-ethnicity.In spite of the uncertainties of the cause of CRC dispar-

ty by race, some organizations recommend blacks shouldtart screening for CRC at age 4014 or 45,15,16 whereasthers recommend average risk screening at age 50 re-ardless of race-ethnicity.17-19 These race-based differ-

ences in CRC screening recommendations create confu-sion for healthcare providers in the delivery of screeningservices to their patients and complicate the measurementof the quality of services provided. For instance, Goodwinet al20 recently reported that blacks among the Medicarepopulation were more likely to undergo early repeatscreening after a negative colonoscopy, which is an over-use of limited healthcare resources. It is unclear if thisoveruse is related to the suggestion that blacks were morelikely to receive substandard care21-23 and perhaps moreikely to have missed lesions at colonoscopy.

To date, most studies evaluating white–black differ-nces in CRC risk have focused on differences in neoplasiarevalence,1,2,4-7 but another measure of biological sus-eptibility is the risk of recurrence after polypectomy.sing data from the Polyp Prevention Trial (PPT) and theolyp Prevention Trial Continued Follow-up Study (PPT-FS), we assessed whether blacks were more likely toave adenomas that were missed at baseline colonoscopy.e also evaluated the risk of adenoma and advanced

denoma recurrence over 4 years (PPT) and the cumula-ive recurrence risk over a maximal follow-up period of 12ears (PPT and PPT-CFS).

METHODS

Study populationThe design and results of the PPT are published

elsewhere.24-26 In summary, the PPT was a 4-year multi-enter, randomized, controlled trial that evaluated the ef-ect of a low-fat, high-fiber, fruit and vegetable diet on theisk of colorectal adenoma recurrence. A total of 2079articipants who were at least 35 years old and had one or

ore histologically confirmed adenomatous polyps re- t

448 GASTROINTESTINAL ENDOSCOPY Volume 77, No. 3 : 2013

oved within 6 months were randomized between June991 and January 1994. The clinical trial was approved byhe institutional review boards of the National Cancernstitute and each of the eight participating clinical cen-ers. All participants gave written informed consent. Therial was completed in 1998.

After the trial ended, 1297 subjects participated in aassive continued follow-up study (PPT-CFS) intended toscertain the long-term effect of the dietary interventionuring the trial on subsequent adenoma recurrence. Thextended follow-up began in 1995 and ended in 2004. Theurrent study was a secondary analysis of deidentified datarom the PPT and PPT-CFS. Final approval for the currenttudy was obtained from the National Cancer Institute onuly 11, 2012.

xposure and outcome assessmentAt baseline, characteristics of the participants, including

elf-identified race-ethnicity and health-related lifestyle,ere obtained through interviews. Per design and proto-ol of the PPT, dietary counseling took place in the clinicalenters, whereas colonoscopic examinations were per-ormed by community gastroenterologists and hence re-ected the performance of colonoscopy in community-ased practice. The participants underwent a clearingolonoscopy approximately 1 year after randomizationT1) to remove any lesion that may have been missed atualifying colonoscopy (T0). Participants were followedor 4 years after randomization and had an end-of-trialT4) colonoscopy to ascertain adenoma recurrence. Anydenoma found during an incidental colonoscopy afterhe T1 examination (ie, outside the PPT protocol) wasonsidered to be recurrent. For the PPT-CFS participants,ost-trial colonoscopies were performed per routine cares determined by the participants’ care providers. Theeports of the first colonoscopy performed after the trialere included in this analysis. The colonoscopy reportsrovided information on size, number, and location ofolyps. The histology and degree of dysplasia during theain PPT trial were confirmed by two central gastrointes-

inal trial pathologists, but the histopathology determina-

Take-home Message

● When the utilization and quality of surveillancecolonoscopy performed after adenoma removal is similaramong non-Hispanic blacks and non-Hispanic whites,there may not be any meaningful difference in the risk ofadenoma and advanced adenoma recurrence to warrantdifferent postpolypectomy surveillance practice patternsbased on race-ethnicity.

● Increasing frequency of surveillance colonoscopy amongnon-Hispanic blacks may not be an effective strategy toreduce colorectal cancer disparity.

ions during PPT-CFS were made by the community pa-

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Laiyemo et al Race and adenoma recurrence

thologists where the colonoscopies took place. Wedefined an advanced adenoma as an adenoma withsize � 1 cm in diameter or villous histology or high-gradedysplasia or invasive cancer.

A total of 1905 participants (91.6%) completed the trialby undergoing the end of trial (T4) colonoscopy and 774(59.7%) of PPT-CFS enrollees (n � 1297) had a colonos-copy during the extended follow-up period. The dietaryintervention did not affect adenoma recurrence during thePPT26 or during the PPT-CFS.27 Our analytic cohort for thistudy comprises 1668 non-Hispanic white (whites) and53 non-Hispanic black (blacks) participants who com-leted the trial and had complete information on the

ocation of their baseline adenoma and 688 white and 55lack enrollees in the PPT-CFS who had at least oneolonoscopy subsequent to the trial (Fig. 1). We excludedll Hispanics (whites and blacks) and other races (Asiansnd Native Americans) from this analysis.

Statistical analysesWe compared the baseline demographic, lifestyle, and

baseline adenoma characteristics of PPT participants byrace-ethnicity (whites vs blacks). We also compared the

Figure 1. Diagram of flow o

characteristics of PPT-CFS participants to nonparticipants (

www.giejournal.org V

y race-ethnicity. We used the Wilcoxon rank-sum (Mann-hitney) test to compare age as a continuous variable and

sed the chi-square test to compare categorical variables.e analyzed the rate of missed adenoma (defined by

PT protocol as adenoma found at T1 colonoscopy) byace-ethnicity as a quality measure because of the sug-estion in the literature that substandard care receivedy blacks is a substantial contributor to health dispari-ies by race-ethnicity.21-23 We used Poisson regressionodels with robust standard error estimation to com-are the risk of missed adenoma (T1) versus no misseddenoma by race-ethnicity. We also compared the riskf adenoma recurrence versus no adenoma recurrencet the end of the PPT (T4).

We defined adenoma recurrence as adenomas foundubsequent to the T1 clearing colonoscopy. For the 127articipants who did not undergo T1 clearing colonos-opy, any adenoma at colonoscopy after 2 years from theaseline examination was regarded as recurrent per PPTrotocol. Assuming an adenoma recurrence rate of 35%mong whites, our study had 80% power to detect a 33%ncreased risk of recurrence among blacks. We calculatedncidence risk ratios (RR) and 95% confidence intervals

ticipants through the study.

CI). We used multinomial logistic regression models to

olume 77, No. 3 : 2013 GASTROINTESTINAL ENDOSCOPY 449

Page 4: Short- and long-term risk of colorectal adenoma recurrence among whites and blacks

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Race and adenoma recurrence Laiyemo et al

evaluate adenoma recurrence by colon subsite. We cate-gorized adenoma recurrence by colon subsite location asno recurrence, distal-only recurrence, or at least one prox-imal recurrence and calculated the relative risk ratio (RRR)and 95% CI. Advanced adenoma recurrence by colonsubsite was categorized in a similar fashion.

Because of the suggestion that CRC occurs at an earlierage among blacks,11 we performed an exploratory analysisamong participants who were younger than 50 years atbaseline. We also performed a sensitivity analysis in whichwe added adenomas removed at T1 clearing colonoscopyto the T4 colonoscopy (as recurrent lesions) and repeatedour analyses. Finally, we compared the cumulative ade-noma recurrence (T1 plus T4 plus PPT-CFS colonoscopyfindings) by race-ethnicity among PPT-CFS participants.Assuming a cumulative adenoma recurrence rate of 60%among whites, our study had 88% power to detect a 33%increased risk of cumulative adenoma recurrence amongblacks.

We included age, sex, randomization assignment, bodymass index, highest education attained (as a surrogate forsocioeconomic status), use of nonsteroidal anti-inflammatorydrugs, smoking, and family history of CRC in our final mul-tivariable models. For the end-of-PPT analysis, we had infor-mation on whether the cecum was reached during colonos-copy and on the adequacy of bowel preparation. These werealso added to the multivariable models. We used Stata statis-tical software, version 11.2 (StataCorp, College Station, TX)for our analyses. All reported P values correspond to two-sided tests.

RESULTS

Baseline characteristics in PPTA total of 1668 whites (91.6%) and 153 blacks (8.4%)

had information on the location of their baseline adenomaand completed the 4-year trial. Table 1 shows selectedbaseline characteristics of study participants by race-ethnicity. When compared with whites, blacks had lessformal education and were more likely to be obese, butthere were no differences in age or sex. Black participantsin the trial had a higher prevalence of advanced adenomaat baseline (44.4% vs 37.0%; P � .07). Of note, there wasno difference by race-ethnicity in the number of peoplewho failed to complete the PPT (8.3% whites vs 9.9%blacks, P � .47).

Missed adenoma and advanced adenomaOf 1821 participants in the current study, 1694 (93.0%)

underwent the clearing (T1) colonoscopy designed perPPT protocol to remove any missed adenoma approxi-mately 1 year after randomization. There was no differ-ence in the receipt of T1 colonoscopy by race-ethnicity(1552 whites [93.1%] vs 142 blacks [92.8%]; P � .91).lacks and whites had similar risks of missed adenoma

nd advanced adenoma (Table 2). f

450 GASTROINTESTINAL ENDOSCOPY Volume 77, No. 3 : 2013

denoma and advanced adenoma recurrencen PPT (short term)

At the end-of-trial (T4) colonoscopy, cecal intubationas documented for 151 blacks (98.7%) versus 1591hites (95.4%) (P � .054), and bowel preparation wasocumented as adequate for 153 blacks (100%) versus619 whites (97.1%) (P � .032). However, information onhe degree of adequacy of the bowel preparation, such asood or excellent bowel preparation, was not available.denoma recurrence occurred among 717 participants39.4%), and 120 participants (6.6%) had advanced ade-oma recurrence. Overall, the recurrence rates were sim-lar by race-ethnicity (Table 3). A total of 60 blacks (39.2%)nd 657 whites (39.4%) had adenoma recurrence (RR �98; 95% CI, .80-1.20), whereas 13 blacks (8.5%) and 107hites (6.4%) had advanced adenoma recurrence (RR �.18; 95% CI, .68-2.05). There was no difference in theecurrence of adenoma and advanced adenoma by colonubsite (Table 3).

denoma recurrence among participantsounger than age 50 years at baselineNo previous study has evaluated adenoma recurrence

isk by race-ethnicity among those younger than age 50ears. Therefore, we conducted an exploratory analysis inhis regard. There were a total of 230 participants: 213hites and 17 blacks. No age difference was found be-

ween the two groups (mean age of whites, 44.1 years, vsean age of blacks, 44.3 years; P � .98). We observed a

ower adenoma recurrence among blacks (1 black [5.9%]s 50 whites [23.5%]; P � .093), but there was no signifi-ant difference in the risk of recurrence by race-ethnicityn the multivariable model (RR � .24; 95% CI, .04-1.60).

ensitivity analysisAlthough adenoma found at T1 colonoscopies were

egarded as missed lesions in PPT, there is also a possibil-ty that these lesions may be new. Therefore, we per-ormed a sensitivity analysis and added adenoma found at1 to T4 adenoma and repeated our analysis. This did nothange the results by race-ethnicity. The adenoma recur-ence rate was 56.2% among blacks and 54.4% amonghites (RR � 1.03; 95% CI, .89-1.19), and advanced ade-oma recurrence rate was 12.4% among blacks and 10.5%mong whites (RR � 1.16; 95% CI, .77-1.76).

umulative adenoma and advanced adenomaecurrence in PPT-CFS (long term)

No difference in participation was found in the PPT-CFSy race-ethnicity. A total of 95 black (62.1%) and 1140hite (68.4%) PPT completers agreed to participate in

he PPT-CFS (P � .113). Of PPT-CFS enrollees, no dif-erence was found in the receipt of post-trial colonos-opy by race-ethnicity: 55 blacks (36.0%) and 688hites (41.3%) had another colonoscopy during the

ollow-up period (P � .64). The comparison of the

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Page 5: Short- and long-term risk of colorectal adenoma recurrence among whites and blacks

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Laiyemo et al Race and adenoma recurrence

baseline characteristics of these PPT-CFS participants byrace-ethnicity was similar to the race-ethnicity compar-ison of the entire cohort included in this analysis except

TABLE 1. Baseline characteristics of PPT and PPT-CFS participa

Characteristics

Non-Hispanicwhites

(n � 1668)

Mean age, yr (SD) 61.3 (9.9)

Randomization assignment, n (%)

Control 843 (50.5)

Intervention 825 (49.5)

Sex, n (%)

Female 600 (36.0)

Male 1068 (64.0)

Education, n (%)*

High school or less 396 (23.8)

More than high school 1271 (76.2)

Body mass index, kg/m2, n (%)†

�25 448 (26.9)

25-29 791 (47.4)

�30 429 (25.7)

Smoking, n (%)

Never 658 (39.5)

Former 797 (47.8)

Current 213 (12.8)

Positive first-degree family history of coloncancer, n (%)

457 (27.4)

Nonsteroidal anti-inflammatory drugs at leastonce a month, n (%)

573 (34.4)

Baseline adenoma, n (%)

�3 synchronous adenomas 252 (15.1)

Advanced adenoma‡ 617 (37.0)

Baseline adenoma location, n (%)

Distal only 927 (55.6)

Proximal only 447 (26.8)

Synchronous proximal and distaladenomas

294 (17.6)

PPT, Polyp Prevention Trial; PPT-CFS, Polyp Prevention Trial Continued Follow-*Missing education status for one white participant.†Highest body mass index in PPT � 38.8 kg/m2.‡Advanced adenoma � size �1 cm in diameter or villous histology or high-gr

that the difference in the highest education attained, our f

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arker for socioeconomic status, was no longer signif-cantly different (Table 1).

Including the 4-year trial period, the cumulative mean

race-ethnicity

PPT-CFS

ispanicacks

153) P value

Non-Hispanicwhites

(n � 688)

Non-Hispanicblacks

(n � 55) P value

8 (9.5) .53 59.9 (8.8) 58.7 (8.8) .29

(43.1) .08 341 (49.6) 23 (41.8) .27

(56.9) 347 (50.4) 32 (58.2)

(33.3) .52 235 (34.2) 16 (29.1) .45

(66.7) 453 (65.8) 39 (70.9)

(35.3) .002 132 (19.2) 16 (29.1) .077

(64.7) 556 (80.8) 39 (70.9)

(18.3) .006 172 (25.0) 10 (18.2)

(45.1) 346 (50.3) 23 (41.8) .043

(36.6) 170 (24.7) 22 (40.0)

(31.4) .055 283 (41.1) 16 (29.1)

(50.3) 333 (48.4) 31 (56.4) .194

(18.3) 72 (10.5) 8 (14.6)

(22.2) .167 225 (32.7) 16 (29.1) .58

(29.4) .22 227 (33.0) 22 (40.0) .29

(10.5) .12 92 (13.4) 5 (9.1) .36

(44.4) .069 269 (39.1) 20 (36.4) .69

(48.4) 387 (56.3) 23 (41.8)

(32.7) .198 188 (27.3) 22 (40.0) .086

(19.0) 113 (16.4) 10 (18.2)

dy.

splasia or invasive cancer.

nts by

PPT

Non-Hbl

(n �

60.

66

87

51

102

54

99

28

69

56

48

77

28

34

45

16

68

74

50

29

up Stu

ollow-up period among PPT-CFS participants was 8.3

olume 77, No. 3 : 2013 GASTROINTESTINAL ENDOSCOPY 451

Page 6: Short- and long-term risk of colorectal adenoma recurrence among whites and blacks

lawctysnadmhdm

Race and adenoma recurrence Laiyemo et al

years (range, 4.9-12.4 years). The total mean follow-upperiod was similar among blacks and whites (8.5 yearsamong blacks vs 8.3 years among whites; P � .50). A totalof 37 blacks (67.3%) and 461 whites (67.0%) had at leastone adenoma recurrence during the entire follow-up pe-riod. There was no difference in the cumulative adenomaand advanced adenoma recurrence by race-ethnicity(Table 4). The sample size was too small for a mean-ingful analysis of recurrence by colon subsite.

DISCUSSION

We compared the risk of adenoma and advanced ade-noma recurrence among white and black PPT participants

TABLE 2. Risk of missed adenoma and missed advanced adeno

Race-ethnicity

No missedadenoma

n (%)

Any missedadenoma

n (%)

Misseno mi

R

White (n � 1552) 1010 (65.1) 542 (34.9) R

Black (n � 142) 94 (66.2) 48 (33.8) .9

Adjusted for age, sex, randomization assignment, education, body mass indexcolorectal cancer.RR, Incidence risk ratio.

TABLE 3. Risk of adenoma and advanced adenoma recurrence

Characteristics

No adenoma recurrence, n (%)

Any adenoma recurrence, n (%)

Any adenoma recurrence vs no recurrence, RR (95% CI)

Any advanced adenoma recurrence, n (%)

Any advanced adenoma recurrence vs no recurrence, RR (95% CI)

Distal only adenoma recurrence, n (%)

Distal only adenoma recurrence vs no recurrence, RRR (95% CI)

Any proximal adenoma recurrence, n (%)

Any proximal adenoma recurrence vs no recurrence, RRR (95% CI)

Distal only advanced adenoma recurrence, n (%)

Distal only advanced adenoma recurrence vs no recurrence, RRR (9

Any proximal advanced adenoma recurrence, n (%)

Any proximal advanced adenoma recurrence vs no recurrence, RRR

Adjusted for age, sex, randomization assignment, education, body mass indexcolorectal cancer, cecum reached during colonoscopy, and adequacy of boweRR, Incidence risk ratio; RRR, relative risk ratio.

in the short term (4 years) with PPT-CFS participants in the c

452 GASTROINTESTINAL ENDOSCOPY Volume 77, No. 3 : 2013

ong term (maximal follow-up, 12 years) and did not findny racial difference in the risk of recurrence. It is note-orthy that the uptake of surveillance colonoscopy wasomparable between blacks and whites. Furthermore,here was no difference in adenoma detection within aear of index colonoscopy by race-ethnicity. Our studyuggests that the observed disparity in CRC by race mayot be due to increased susceptibility to carcinogenesismong blacks, at least in the early phase of neoplasticisease. Our findings do not provide evidence to supportore frequent surveillance for blacks with a personalistory of adenoma as an intervention to reduce CRCisparity. The implication of our findings is that blacksay not need a different postpolypectomy surveillance

T1 colonoscopy by race-ethnicity

noma vsdenoma

CI)

Missed advancedadenoma

n (%)

Missed advancedadenoma vs no missed

adenomaRR (95% CI)

nce 93 (6.0) Reference

-1.22) 8 (5.6) .97 (.49-1.91)

f nonsteroidal anti-inflammatory drugs, smoking, and family history of

ce-ethnicity in the 4-year Polyp Prevention Trial

Non-Hispanic whites(n � 1668)

Non-Hispanic blacks(n � 153)

1011 (60.6) 93 (60.8)

657 (39.4) 60 (39.2)

Reference .98 (.80-1.20)

107 (6.4) 13 (8.5)

Reference 1.18 (.68-2.05)

205 (12.3) 15 (9.8)

Reference .78 (.44-1.38)

452 (27.1) 45 (29.4)

Reference 1.05 (.71-1.54)

42 (2.5) 5 (3.3)

I) Reference 1.14 (.43-3.01)

64 (3.8) 8 (5.2)

CI) Reference 1.31 (.59-2.91)

f nonsteroidal anti-inflammatory drugs, smoking, family history ofaration.

ma at

d adessed aR (95%

efere

7 (.77

, use o

by ra

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Laiyemo et al Race and adenoma recurrence

Three domains of CRC disparities have been identified:healthcare access, which includes availability of healthinsurance, accessible facilities, and providers; healthcareutilization, which entails the use of healthcare resourceswhen it is available; and biological differences.28 We pre-iously evaluated two domains, healthcare utilization andiology, within the same cohort of subjects in a screeningopulation.29 In that study we used data from the recentlyoncluded Prostate, Lung, Colorectal, and Ovarian Cancercreening Trial and evaluated CRC disparity by race-thnicity by examining the rate of diagnostic colonoscopyfter an abnormal screening flexible sigmoidoscopymong 57,561 white and 3011 black participants. A com-arable rate was found of finding polyps or masses duringexible sigmoidoscopy screening among whites andlacks (23.9% vs 25.5%, respectively; P � .26) at screening,ut blacks were less likely to undergo diagnostic colono-copy (RR � .88; 95% CI, .83-.93) within a year of thebnormal screening. However, when compared withhites, blacks had comparable yield of adenoma (RR �.01; 95% CI, .92-1.11), advanced adenoma (RR � 1.11;5% CI, .94-1.30), and CRC (RR � 1.58; 95% CI, .80-3.12)mong those who underwent diagnostic colonoscopy.hat study suggested that healthcare utilization may belaying more of a role in the observed CRC disparity byace. Taken together, the aforementioned study and theurrent study provide some evidence that blacks may note more susceptible to colorectal carcinogenesis thanhites in terms of prevalence and recurrence of precursor

esions of CRC.We are only aware of two studies that have compared

he risk of adenoma recurrence between blacks andhites. Using data from the adenoma pooling project,artínez et al30 reported a similar risk of adenoma recur-

rence among blacks and whites over a median of 47.2months of follow-up (odds ratio � 1.12; 95% CI, .92-1.37)for nonadvanced and (odds ratio � 1.08; 95% CI, .79-1.47)for advanced adenoma, but the authors did not report onthe risk of recurrence by colon subsite. Using retrospectivedata collection, Penn et al31 reported that race was notassociated with the prevalence of polyps at baseline (odds

TABLE 4. Cumulative risk of adenoma and advanced adenomafollow-up of 8.3 years (range, 4.9-12.4 years)

Race-ethnicity

No adenomarecurrence

n (%)

Adenomarecurrence

n (%)

Adenoma vadenoma recu

RR (95%

White (n � 688) 227 (33.0) 461 (67.0) Referenc

Black (n � 55) 18 (32.7) 37 (67.3) 1.01 (.84-1

Adjusted for age, sex, randomization assignment, education, body mass indexcolorectal cancer.PPT, Polyp Prevention Trial; PPT-CFS, Polyp Prevention Trial Continued Follow-

ratio � 1.04; 95% CI, .85-1.28). However, among 57 pa- h

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ients (7 blacks) with baseline adenoma who had aollow-up colonoscopy after a median of 3.6 years later,ace was not associated with polyp recurrence (hazardatio � 1.89; 95% CI, .68-5.24). This study was limited byts retrospective design, lack of histopathological diagnosisor all patients with the use of polyps as a proxy foreoplasia, small sample size for the postpolypectomy co-ort (with only 7 blacks), and short follow-up interval. Inur observational study using data from a completed ran-omized trial, we did not find any difference in the risknd location of adenoma and advanced adenoma recur-ence among blacks and whites despite a higher preva-ence of advanced adenoma among blacks at baseline.here was no difference in recurrence risk over a maximalollow-up period of 12 years.

Our study has many notable strengths. Our study pop-lation is from a large randomized controlled trial witharticipants recruited from geographically disperse areas,edicated central pathologists with expertise in gastroin-estinal tumors examined the adenomas, and all patientsad planned colonoscopic assessment for recurrence aftern adequate follow-up period of 4 years. Furthermore, weere able to assess recurrence among a subset of the studyopulation over a maximum follow-up of 12 years.Our study also has some limitations. The participants in

he PPT were self-selected and may be healthier thanomparable members of the general population. We had aelatively small number of blacks, particularly in the long-erm follow-up study; therefore, our study power wasimited to detect a 33% increased risk of adenoma recur-ence among blacks. Finally, we did not have any infor-ation about serrated lesions because it was not a well-nown phenomenon at the time the trial was conducted.owever, we are not aware of any conclusive evidence

hat blacks are more likely than whites to have sessileerrated adenomas that could potentially advance to CRChrough an alternate pathway.

In conclusion, we did not find an increased risk ofdenoma and advanced adenoma recurrence amonglacks as compared with whites. Our study does not sup-ort more frequent surveillance for blacks with personal

rence by race-ethnicity in PPT and PPT-CFS over a mean

ceAdvanced adenoma

recurrencen (%)

Advanced adenoma recurrencevs no adenoma recurrence

RR (95% CI)

116 (16.9) Reference

8 (14.5) 1.03 (.60-1.79)

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, use o

istory of adenoma as an intervention to reduce CRC

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Race and adenoma recurrence Laiyemo et al

disparity. Rather, our study suggests that when the uptakeand quality of colonoscopy performed are equal, blacksmay not be at an increased risk for CRC to warrant differ-ent guideline recommendations. However, further studiesare needed to elucidate the underlying factors for theincreased burden of CRC among blacks and to possiblyidentify a subset of blacks at increased biological suscep-tibility to CRC.

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edical Center, Dallas, Texas (6), Division of Gastroenterology, Departmentf Medicine, Georgetown University, Washington, DC (7), Laboratory of Can-er Prevention, Center for Cancer Research, National Cancer Institute, Na-ional Institutes of Health, Bethesda, Maryland (8), Department of Medicine,

eharry Medical Center, Nashville, Tennessee (9), Department of Epidemi-logy, Johns Hopkins Bloomberg School of Public Health, Baltimore, Mary-

and (10), Nutritional Epidemiology Branch, Division of Cancer Epidemiol-gy and Genetics, National Cancer Institute, National Institutes of Health,ethesda, Maryland (11).

resented at Digestive Disease Week, May 19-22, 2012, San Diego, Cali-ornia (Gastroenterology 2012;142:S408).

eprint requests: Adeyinka O. Laiyemo, MD, MPH, Division of Gastroenter-logy, Department of Medicine, Howard University College of Medicine,041 Georgia Avenue, NW, Washington, DC 20060.

f you would like to chat with an author of this article, you may contact Dr

aiyemo at [email protected].

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