Longitudinal Adherence to Fecal Occult Blood Testing Impacts Colorectal Cancer Screening Quality

© 2011 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY

see related editorial on page x

INTRODUCTION In 2009, 75,590 men and 71,380 women were diagnosed with

colorectal cancer (CRC), making it the third most commonly

diagnosed cancer among men and women in the United States

( 1 ). Fortunately, the incidence and mortality rates for CRC are

decreasing, in large part because of the increasing utilization of

screening tests in the population ( 2 ).

Multiple modalities are currently available to screen for CRC

( 3 ). Fecal occult blood testing (FOBT) has demonstrated mortal-

ity benefi t in randomized controlled trials ( 4 – 6 ), and as such has

remained a major tool for CRC screening for decades. Although

the use of FOBT is decreasing in private health-care settings

( 7,8 ), it remains widely utilized in a number of large integrated

medical systems, including the Veterans Health Administration

(VHA) ( 9 ).

Because annual testing is recommended to maintain program-

matic eff ectiveness ( 3,10,11 ), longitudinal adherence is a critical

component of FOBT-based screening programs. However, little

is known regarding rates of longitudinal adherence with FOBT

outside of clinical trials. Existing quality measures, such as the

Healthcare Eff ectiveness Data and Information Set (HEDIS) ( 12 )

and the VHA Performance Measures ( 13 ), assess receipt of FOBT

over the recommended interval only (i.e., within the past year)

and disregard adherence with repeated testing. As such, these

measures may overestimate the success of CRC screening pro-

grams if adherence to repeated testing is low. Our specifi c aim

in this study was to measure the degree of adherence to repeated

FOBTs in the VHA in order to better understand the impact of

longitudinal adherence on the programmatic eff ectiveness of

CRC screening.

Longitudinal Adherence to Fecal Occult Blood Testing Impacts Colorectal Cancer Screening Quality Ziad F. Gellad , MD, MPH 1 , 2 , Karen M. Stechuchak , MS 1 , Deborah A. Fisher , MD, MHS 1 , 2 , Maren K. Olsen , PhD 1 , 3 , Jennifer R. McDuffi e , PhD, RD, MPH 1 , Truls Ø stbye , MD, MPH, PhD 4 , 5 and William S. Yancy Jr , MD, MHS 1 , 2

OBJECTIVES: Existing cross-sectional quality measures for colorectal cancer (CRC) screening do not assess longitudinal adherence and thus may overestimate the quality of care. Our goal was to evaluate the adherence to repeated yearly fecal occult blood tests (FOBTs) in order to better understand the extent to which longitudinal adherence may impact screening quality.

METHODS: This was a retrospective cohort analysis of 1,122,645 patients aged 50 – 75 years seen at any of the 136 Department of Veterans Affairs medical centers across the United States in 2000 and followed through 2005. The primary outcome was receipt of adequate CRC screening as defi ned by receipt of FOBTs in at least 4 out of 5 years or receipt of any number of FOBTs in addition to at least one colonoscopy, fl exible sigmoidoscopy, or double-contrast barium enema. In a predefi ned subset of patients receiving exclusively FOBT, adherence with repeated testing was determined over the 5-year study period.

RESULTS: Only 41.1 % of men and 43.6 % of women received adequate screening. Of the 384,527 men who received exclusively FOBT, 42.1 % received a single FOBT, 26.0 % received 2 tests, 17.8 % received 3 tests, and only 14.1 % were documented to have received at least 4 tests during the study period. Among the 10,469 female veterans receiving FOBT alone, rates were similar with only 13.7 % completing at least 4 FOBTs in the 5-year study period.

CONCLUSIONS: Adherence to repeated FOBT is low, suggesting that cross-sectional measurements of quality may overestimate the programmatic success of CRC screening.

Am J Gastroenterol 2011; 106:1125 – 1134; doi: 10.1038/ajg.2011.11 ; published online 8 February 2011

1 Center for Health Services Research in Primary Care, Department of Veterans Affairs Medical Center , Durham , North Carolina , USA ; 2 Department of Medicine, Duke University Medical Center , Durham , North Carolina , USA ; 3 Department of Biostatistics and Bioinformatics, Duke University Medical Center , Durham , North Carolina , USA ; 4 Department of Community and Family Medicine, Duke University Medical Center , Durham , North Carolina , USA ; 5 Duke-NUS Graduate Medical School , Singapore . Correspondence: Ziad F. Gellad, MD, MPH , Division of Gastroenterology, Duke University Medical Center , Box 3913, Durham , North Carolina 27710 , USA . E-mail: [email protected] Received 4 November 2010; accepted 4 January 2011

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1125 ORIGINAL CONTRIBUTIONS nature publishing group

Gellad et al.

The American Journal of GASTROENTEROLOGY VOLUME 106 | JUNE 2011 www.amjgastro.com

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METHODS Data sources and patients Th is retrospective cohort was originally assembled for a study

examining the relationship between obesity and the receipt of

clinical services within the VHA ( 14 ). Th is study was approved

by the Durham VHA Medical Center institutional review board.

Data used to defi ne the study sample were gathered by the VHA

HAIG (Health Analysis and Information Group), which obtained

data extracted from the electronic medical records at 136 VHA

facilities nationwide (see Figure 1 ). Th e initial data set contained

2,347,335 patients with body weight data recorded in fi scal year

2000 (1 October 1999 to 30 September 2000). Th e study period

extended to the end of fi scal year 2005 (September 2005).

Main sample . Th is data set was merged with VHA administrative

databases including demographic (VHA Vital Status Mini fi le and

Outpatient Clinic (OPC)) and clinical data (OPC, Patient Treat-

ment (PTF), Fee Basis, and Pharmacy Decision Support System)

fi les. VHA Vital Status Mini fi le combines death dates from PTF,

Benefi ciary Identifi cation Records Locator Subsystem, Medicare

Vital Status, and Social Security Administration death fi les. OPC

contains records for all VA outpatient encounters such as clinic

visits and outpatient procedure visits. PTF contains records for

all VA hospitalizations. Fee basis fi les contain utilization infor-

mation on non-VA-provided health-care services authorized

and paid for by the VA under the VA ’ s Fee Basis program. We

excluded records that did not have a matching identifi er when

cross-checked with the Vital Status Mini fi le.

Within this sample, we further refi ned the study population by

limiting our analysis to men and women aged 50 – 75 years to mir-

ror the eligible population for the VHA and HEDIS performance

measures for CRC screening. We excluded patients with a diag-

nosis of CRC in the year before and including the inception date

or those who developed CRC during the study period. Finally,

we excluded patients who died during the study period. Th e fi nal

sample consisted of 1,091,570 men and 31,075 women.

Subgroup samples . We further categorized the fi nal sample by

primary screening modality in an attempt to identify a subgroup

of patients whose primary means of screening was FOBT. Th us,

the FOBT-primary subgroup describes those patients whose fi rst

screening test within the study period was an FOBT ( n = 571,544).

In the FOBT-primary subgroup, we did not include those patients

who had sigmoidoscopy, colonoscopy, or barium enema on the

same day or before any FOBT ( n = 229,471) or those patients

who had no CRC screening test documented in the study period

( n = 321,630). A subset of the FOBT-primary subgroup was fur-

ther defi ned by identifying patients whose only screening test(s)

during the study period was FOBT; this group of patients was re-

ferred to as the FOBT-only subgroup ( n = 394,996). Th e goal of this

classifi cation was to eliminate those patients who may not have

returned for an FOBT because they had a positive test.

Data collection and measurement Outcome variables . We assessed the receipt of CRC screening tests

during the 5-year study window. Current Procedural Terminology

(CPT) codes were drawn from outpatient event fi les and Fee Basis

Files; ICD-9 (International Classifi cation of Diseases, 9th Revision)

procedure codes were drawn from VHA procedure fi les, VHA sur-

gery fi les, VHA observation fi les, non-VHA procedure fi les, and

non-VHA surgery fi les; ICD-9 V codes were drawn from outpatient

event fi les and fee basis fi les. A test was considered “ received ” if a

corresponding procedure code was present for that patient in the

electronic databases. Because these preventive services are prima-

rily performed in outpatient clinics, the VHA inpatient databases

were not searched with the exception of colonoscopy because

some patients might have been admitted to the hospital for this

procedure. Acceptable tests included the following:

Patients with weight recorded in FY2000 (n= 2,347,335)

Included in final analysis(n=1,122,645)

Excluded records: - Age <50 (n= 453,803) - Age ≥76 (n= 407,193) - Died during remaining study period (n= 215,952) - Diagnosed with CRC before or during study period (n= 25,060)

Excluded records: - Height and/or weight inconsistent between measurements; BMI out of range; or both weight and height out of range or missing (n= 3,738) - No matching record when merged with confirmatory databases; gender unknown; age <18 (n= 13,294) - Died in first 8 months of study period (n= 105,650)

Usable records (n= 2,224,653)

Figure 1 . Overview of analysis sample. BMI, body mass index; CRC, colorectal cancer; FY, fi scal year.

Longitudinal Adherence to Fecal Occult Blood Testing


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1. FOBT: CPT 82270, 82274

2. Barium enema: CPT 74270, 74280

3. Sigmoidoscopy: CPT 45330 – 31, 45333 – 34, 45337 – 45339

4. Colonoscopy: CPT 44388 – 89, 44392 – 94, 45378, 45380,

45382 – 85; ICD-9 Diagnosis Codes V76.41, V76.50, V76.51;

ICD-9 Procedure Codes 45.23 – 45.25

Although some patients may have received services for rea-

sons other than screening, our goal was to mirror the measure-

ment of colorectal testing use in the VA and HEDIS performance

measures.

Factors potentially associated with receipt of preventive services .

Several factors that may relate to receipt of adequate screening

were selected for inclusion in the multivariable models. Subject

characteristics included: age, gender, body mass index race /

ethnicity (Non-Hispanic White, Non-Hispanic Black, Other, and

Unknown), marital status (married, other, or unknown), outside

insurance (none or any), health-care service eligibility (4 levels

based on income and military service-related disabilities), geo-

graphic region (by subjects ’ home Veterans Integrated Service

Network) ( 15 ), and whether the patient was assigned a primary

care practitioner in the VHA (according to the 2000 Primary

Care Management Module). Health status was represented by the

Charlson Comorbidity Index (coded 0, 1, 2, or ≥ 3) ( 16,17 ) using

inpatient and outpatient diagnostic codes from the year before

and including the index date.

Statistical analysis . Th e primary outcome for our analysis was

receipt of adequate screening . A patient was considered to be

adequately screened if s / he received the appropriate number

of screening procedures during the entire 5-year period of fol-

low-up based on the recommended intervals of screening, i.e.,

yearly FOBT in 4 out of 5 years, any number of FOBTs followed

or preceded by barium enema, sigmoidoscopy, or colonoscopy,

or one of these three procedures without FOBT ( 3 ). For FOBT

testing interval, we chose an “ appropriate ” time interval of 8

months, which is less than the recommended yearly interval, to

account for the possibility of a patient receiving the service ear-

ly because of the timing of their clinic appointments, but long

enough to avoid counting possible repeat testing for abnormal

screening results. We did not require patients to complete fi ve

FOBTs over 5 years because of the possibility that the last FOBT

would fall outside the study window as a result of the timing of

clinic appointments.

Simple descriptive statistics were used to report screening rates.

Within the FOBT-only subgroup, we examined the likelihood of

repeated testing by assessing the proportion of patients receiving 1,

2, 3, or ≥ 4 FOBTs during the 5 years of observation. Multivariable

logistic regression analysis was used to examine the contribution

of demographic, socioeconomic, and health status factors on the

receipt of adequate screening in the complete cohort of subjects

and the FOBT-only subgroup. Separate models were constructed

for men and women given the large discrepancies in sample size

between genders. Subjects with missing values on any of the

predictors were excluded from the adjusted logistic regression

models (i.e., case-wise deletion). SAS Statistical Soft ware,

Version 9.1 (SAS Institute, Cary, NC) was used for all analyses.

RESULTS Patient characteristics Of the 2,347,335 subjects initially screened for the study, 1,122,645

subjects were included in the present analysis as outlined in Figure 1 .

Table 1 describes the baseline characteristics of the 1,091,570 men

included in the analysis. Th e largest percentage of patients (49.1 % )

in the main male sample was non-Hispanic White. Also, 47.0 %

were documented to have outside health insurance, and slightly

more than half (57.4 % ) were enrolled in primary care within the

VHA. Of the men, 313,130 (28.7 % ) received no screening test

during the study period. Of those men receiving any screening

test, 49.4 % received FOBT alone. Th is group did not diff er appre-

ciably from the main sample of men.

Th e baseline patient characteristics for women ( n = 31,075) are

similarly described in Table 1 . As with men, the majority of women

were non-Hispanic White (52.4 % ) and enrolled in primary care

(59.7 % ); 48.8 % had outside health insurance. Also, 8,500 (27.4 % )

women did not receive any screening test during the study period.

Of those women receiving screening, 46.4 % received FOBT testing

alone. Th e FOBT-only subgroup of women was similar in charac-

teristics to the main sample of women.

Adequacy of screening Among men, 41.1 % received adequate CRC screening during

the 5-year study period. Of men receiving adequate screening,

54,196 (12.1 % ) achieved it by FOBT alone whereas the remaining

393,913 (87.9 % ) received either a colonoscopy, sigmoidoscopy, or

barium enema.

Among women, a similar pattern emerged. Of the 31,075

women in the complete cohort, 43.6 % received adequate screen-

ing of whom 1,430 (10.6 % ) achieved it by FOBT alone whereas

the remaining 12,106 (89.4 % ) achieved it through the receipt of an

alternate test.

Table 2 illustrates the results of the multivariable regression

analysis examining predictors of receipt of adequate screening in

the complete cohort. Although many of the variables achieved sta-

tistical signifi cance, few measured covariates had a major impact

on receipt of adequate screening. For example, enrollment in VHA

primary care was predictive of receiving adequate screening in men

(odds ratio (OR) 1.21, 95 % confi dence interval (CI) 1.20 – 1.22) and

women (OR 1.09, 95 % CI 1.04 – 1.14), although the eff ect was not

profound, particularly in women. Geographic variation in receipt

of adequate screening was observed in both men and women. Men

living in the Northeast (OR 0.73, 95 % CI 0.72 – 0.74), Midwest (OR

0.90, 95 % CI 0.89 – 0.91), or West (OR 0.84, 95 % CI 0.83 – 0.84)

were less likely than those living in the South to receive adequate

screening. Similarly, women in the Northeast (OR 0.84, 95 % CI

0.78 – 0.91), Midwest (OR 0.84, 95 % CI 0.78 – 0.90), or West (OR

0.77, 95 % CI 0.72 – 0.81) were also less likely to undergo adequate

screening when compared with those living in the South.

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Table 1 . Characteristics of main sample and FOBT-only subgroup

Characteristic Main sample FOBT-only subgroup

Men a Women b Men Women

N ( % ) 1,091,570 31,075 384,527 10,469

Age, years, mean (s.d.) 63.0 (7.9) 59.3 (7.2) 64.0 (7.8) 60.0 (7.4)

Race / ethnicity, n ( % )

Non-Hispanic white 533,729 (49.1) 16,241 (52.4) 185,498 (48.3) 5,590 (53.4)

Non-Hispanic black 97,080 (8.9) 2,817 (9.1) 30,246 (7.9) 855 (8.2)

Other c 49,788 (4.6) 977 (3.2) 18,993 (4.9) 301 (2.9)

Unknown 407,443 (37.4) 10,946 (35.3) 149,081 (38.8) 3,714 (35.5)

Marital status, n ( % )

Married 680,755 (62.6) 13,140 (42.4) 247,339 (64.4) 4,363 (41.7)

Other 395,358 (36.3) 17,235 (55.6) 132,621 (34.6) 5,935 (56.7)

Unknown 11,910 (1.1) 605 (2.0) 3,856 (1.0) 162 (1.5)

Outside health insurance, n ( % )

No 576,881 (53.0) 15,852 (51.2) 192,833 (50.2) 5,495 (52.5)

Yes 511,097 (47.0) 15,128 (48.8) 190,966 (49.8) 4,965 (47.5)

VA primary care provider, n ( % )

No 465,182 (42.6) 12,533 (40.3) 168,711 (43.9) 4,241 (40.5)

Yes 626,388 (57.4) 18,542 (59.7) 215,816 (56.1) 6,228 (59.5)

Service eligibility, n ( % )

None 694,449 (63.8) 21,754 (70.2) 251,080 (65.4) 7,333 (70.1)

SC < 50 % 244,280 (22.5) 4,806 (15.5) 82,868 (21.6) 1,657 (15.8)

SC > 50 % 140,390 (12.9) 4,218 (13.6) 46,753 (12.2) 1,403 (13.4)

AA / housebound d 8,921 (0.8) 203 (0.7) 3,117 (0.8) 67 (0.6)

Charlson Index, n ( % )

0 555,190 (50.9) 18,825 (60.6) 192,703 (50.1) 6,373 (60.9)

1 180,787 (16.6) 3,679 (11.8) 67,196 (17.5) 1,296 (12.4)

2 205,368 (18.8) 5,686 (18.3) 73,420 (19.1) 1,897 (18.1)

≥ 3 150,225 (13.8) 2,885 (9.3) 51,208 (13.3) 903 (8.6)

BMI, n ( % )

15 to < 18.5 8,570 (0.8) 397 (1.4) 2,756 (0.8) 142 (1.4)

18.5 to < 25 206,124 (20.3) 6,626 (22.7) 73,020 (20.4) 2,274 (23.0)

25 to < 30 419,637 (41.4) 9,084 (31.1) 151,383 (42.3) 3,106 (31.4)

≥ 30 379,107 (37.4) 13,095 (44.8) 130,752 (36.5) 4,359 (44.1)

Region, n ( % )

South 446,500 (41.1) 13,734 (44.4) 157,337 (41.1) 4,547 (43.5)

Northeast 179,409 (16.5) 3,766 (12.2) 72,701 (18.9) 1,343 (12.8)

Midwest 222,737 (20.5) 5,083 (16.4) 70,646 (18.4) 1,602 (15.3)

West 238,948 (22.0) 8,384 (27.1) 83,012 (21.6) 2,964 (28.3)

AA, aid and attendance; BMI, body mass index; FOBT, fecal occult blood test; SC, service connected; VA, Veterans Affairs. a Men have missing data for the following items ( n in complete cohort): race (3,530), marital status (3,574), outside health insurance (3,592), eligibility (3,530), BMI (78,132), and region (3,976). b Women have missing data for the following items ( n in complete cohort): race (94), marital status (95), outside health insurance (95), eligibility (94), BMI (1,873), and region (108). c Other (race) refers to Hispanic, Asian, and American Indian veterans. d AA and housebound benefi ts are available to veterans who have in-home care or who live in nursing homes or assisted living facilities.



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Table 2 . Receipt of adequate CRC screening in main sample

Characteristic Men a Adjusted odds ratio (95 % CI) Women b

Adjusted odds ratio (95 % CI)

Adequate Inadequate Adequate Inadequate

N ( % ) 448,109 (41.1) 643,461 (58.9) 13,536 (43.6) 17,539 (56.4)

Age, years, mean (s.d.)

62.5 (7.7) 63.3 (8.0) 0.99 (0.99 – 0.99) 58.7 (6.9) 59.7 (7.4) 0.98 (0.98 – 0.99)


Non-Hispanic white 233,766 (43.8) 299,963 (56.2) Ref 7,408 (45.6) 8,833 (54.4) Ref

Non-Hispanic black 44,604 (45.9) 52,476 (54.1) 1.05 (1.04 – 1.07) 1,423 (50.5) 1,394 (49.5) 1.12 (1.03 – 1.22)

Other c 18,024 (36.2) 31,764 (63.8) 0.75 (0.73 – 0.76) 442 (45.2) 535 (54.8) 0.91 (0.79 – 1.04)

Unknown 151,195 (37.1) 256,248 (62.9) 0.79 (0.78 – 0.80) 4,249 (38.8) 6,697 (61.2) 0.79 (0.75 – 0.83)


Married 279,002 (41.0) 401,753 (59.0) Ref 5,853 (44.5) 7,287 (55.5) Ref

Other 164,547 (41.6) 230,811 (58.4) 0.997 (0.99 – 1.01) 7,479 (43.4) 9,756 (56.6) 0.95 (0.91 – 1.00)

Unknown 4,035 (33.9) 7,875 (66.1) 0.74 (0.71 – 0.77) 189 (31.2) 416 (68.8) 0.68 (0.56 – 0.82)

Outside health insurance

No 238,599 (41.4) 338,282 (58.6) Ref 6,802 (42.9) 9,050 (57.1) Ref

Yes 208,978 (40.9) 302,119 (59.1) 1.04 (1.03 – 1.05) 6,720 (44.4) 8,408 (55.6) 1.09 (1.04 – 1.15)

VA primary care provider

No 178,557 (38.4) 286,625 (61.6) Ref 5,299 (42.3) 7,234 (57.7) Ref

Yes 269,552 (43.0) 356,836 (57.0) 1.21 (1.20 – 1.22) 8,237 (44.4) 10,305 (55.6) 1.09 (1.04 – 1.14)


None 274,345 (39.5) 420,104 (60.5) Ref 9,210 (42.3) 12,544 (57.7) Ref

SC < 50 % 105,748 (43.3) 138,532 (56.7) 1.12 (1.11 – 1.13) 2,163 (45.0) 2,643 (55.0) 1.06 (0.99 – 1.13)

SC > 50 % 64,295 (45.8) 76,095 (54.2) 1.16 (1.15 – 1.18) 2,084 (49.4) 2,134 (50.6) 1.22 (1.14 – 1.31)

AA / housebound d 3,201 (35.9) 5,720 (64.1) 0.79 (0.75 – 0.83) 65 (32.0) 138 (68.0) 0.65 (0.48 – 0.89)


0 220,509 (39.7) 334,681 (60.3) Ref 8,049 (42.8) 10,776 (57.2) Ref

1 73,825 (40.8) 106,962 (59.2) 1.03 (1.01 – 1.04) 1,520 (41.3) 2,159 (58.7) 0.95 (0.88 – 1.03)

2 87,708 (42.7) 117,660 (57.3) 1.10 (1.09 – 1.11) 2,625 (46.2) 3,061 (53.8) 1.13 (1.06 – 1.20)

≥ 3 66,067 (44.0) 84,158 (56.0) 1.14 (1.12 – 1.15) 1,342 (46.5) 1,543 (53.5) 1.13 (1.04 – 1.23)

BMI, n ( % )

15 to < 18.5 3,040 (35.5) 5,530 (64.5) 0.80 (0.77 – 0.84) 152 (38.3) 245 (61.7) 0.82 (0.66 – 1.01)

18.5 to < 25 81,179 (39.4) 124,945 (60.6) Ref 2,833 (42.8) 3,793 (57.2) Ref

25 to < 30 174,810 (41.7) 244,827 (58.3) 1.12 (1.11 – 1.13) 4,025 (44.3) 5,059 (55.7) 1.06 (0.99 – 1.13)

≥ 30 162,387 (42.8) 216,720 (57.2) 1.14 (1.12 – 1.15) 5,852 (44.7) 7,243 (55.3) 1.04 (0.98 – 1.11)

Region, n ( % )

South 195,750 (43.8) 250,750 (56.2) Ref 6,498 (47.3) 7,236 (52.7) Ref

Northeast 63,893 (35.6) 115,516 (64.4) 0.73 (0.72 – 0.74) 1,561 (41.4) 2,205 (58.6) 0.84 (0.78 – 0.91)

Midwest 92,354 (41.5) 130,383 (58.5) 0.90 (0.89 – 0.91) 2,124 (41.8) 2,959 (58.2) 0.84 (0.78 – 0.90)

West 95,469 (40.0) 143,479 (60.0) 0.84 (0.83 – 0.84) 3,334 (39.8) 5,050 (60.2) 0.77 (0.72 – 0.81)

AA, aid and attendance; BMI, body mass index; CI, confi dence interval; CRC, colorectal cancer; SC, service connected. a Number of observations after case-wise deletion in adjusted logistic regression model for men=1,010,286; C-statistic for model=0.57. b Number of observations after case-wise deletion in adjusted logistic regression model for women=29,124; C-statistic for model=0.58. c Other (race) refers to Hispanic, Asian, and American Indian veterans. d AA and housebound benefi ts are available to veterans who have in-home care or who live in nursing homes or assisted living facilities.

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FOBT adherence In the subgroup of patients who received FOBT testing alone,

Tables 3 and 4 describe the proportion of men and women who

underwent repeated FOBT testing during the study period. Of

the 384,527 men who received exclusively FOBT testing, 42.1 %

received a single FOBT during the study period, 26.0 % received 2

tests, 17.8 % received 3 tests, and only 14.1 % were documented to

have received at least 4 FOBTs. Among the 10,469 female veterans

receiving FOBT alone, 42.9 % received a single test, 26.1 % received

2 tests, 17.3 % received 3 tests, and only 13.7 % completed at least 4

FOBTs in the 5-year study period.

Factors predicting receipt of adequate FOBT testing were varied

between men and women and were of limited clinical signifi cance.

One exception included geographic variation. Men living in the

Midwest (OR 0.81, 95 % CI 0.79 – 0.83) and West (OR 0.82, 95 % CI

0.80 – 0.84) were less likely to receive adequate repeat FOBT test-

ing than those living in the South. Similarly, women living in the

Midwest (OR 0.66, 95 % CI 0.55 – 0.79) and West (OR 0.65 95 % CI

0.56 – 0.75) had lower rates of repeat testing when compared with

women living in the South. In contrast, men living in the north-

east (OR 1.08, 95 % CI 1.05 – 1.11) were marginally more likely

to receive adequate FOBT testing than those living in the South,

although the same fi nding was not detected in women (OR 1.02,

95 % CI 0.86 – 1.22).

DISCUSSION In this longitudinal analysis of over 1 million outpatients, only

41.1 % of men and 43.6 % of women received adequate CRC

screening, defi ned as receipt of at least four FOBTs or receipt of

a fl exible sigmoidoscopy, colonoscopy, or double-contrast barium

enema. Of the 384,527 men and 10,469 women receiving exclu-

sively FOBT, only 1 in 7 received at least 4 FOBTs during the

5-year study period.

Th e proportion of patients receiving adequate screening found

in our sample is lower than the reported screening rate of > 70 %

from within the VHA using existing performance measure defi -

nitions ( 18 ). However, current performance measures do not

consider rates of repeated testing in evaluating screening quality.

As a result, these measures may overestimate the success of CRC

screening programs. Indeed, the very low proportion of repeat

testing in the FOBT-only subgroup provides evidence support-

ing this hypothesis. Furthermore, previous studies of the cost

eff ectiveness of FOBT have demonstrated that the cost eff ective-

ness of the test is highly sensitive to longitudinal adherence ( 19 ).

Th us, any decrement in adherence to repeated testing may have

substantial implications on policy decisions regarding choice of

preferred screening strategy. Th is concern is especially relevant

in health systems where FOBT is a highly utilized screening

test.

Several previous studies have evaluated adherence to yearly

screening tests ( 6,20 – 23 ). Myers et al. ( 20 ) evaluated compliance

rates with FOBT over 2 years among adult members of a Health

Maintenance Organization (HMO). Th ey found that only 23 %

of subjects completed two rounds of screening, with predictors

of adherence including initial adherence and age > 65 years. In

another population study, O ’ Malley et al. ( 21 ) used a targeted

household telephone survey to evaluate adherence with annual

FOBT in women during a 2-year period. Th ey found that only 29 %

of women completed two FOBTs during the study period.

Studies assessing adherence in the setting of clinical trials

demonstrate higher rates of adherence. For example, Th omas

et al. ( 23 ) evaluated longitudinal adherence with annual FOBT

screening in the Minnesota Colon Cancer Control Study. Th ey

found that 74 % of subjects were compliant with FOBT testing

over the 5-year study period, although their analysis was based

on population-level data and not individual subjects. In their

trial of FOBT for CRC screening, Mandel et al. ( 6 ) reported

that only 46 % of subjects in the annually screened group com-

pleted all requested screening cards over 13 years of follow-

up. Given that this trial helped to establish the eff ectiveness of

FOBT screening, this observation suggests that near-perfect

longitudinal adherence may not be required to achieve mortal-

ity reduction in CRC within a population. However, it is logical

that better longitudinal adherence would translate into greater

mortality reduction.

One of the interesting fi ndings in our multivariable analysis is

the geographic variation in screening adequacy and adherence

with repeated FOBT. Geographic variation in CRC screening rates

has been previously reported outside of the VA ( 2,7,24 ). Geo-

graphic variation in health-care utilization has also been reported

within the VA ( 25 ), although to our knowledge, this is the fi rst

study documenting variation in CRC screening. Th is variation is

independent of patient demographic and socioeconomic factors,

suggesting that system-level factors may be important. Th ese fi nd-

ings deserve further study.

Our results should be interpreted in the context of certain limi-

tations. For one, the existing data set used for the study contained

only 5 years of VHA data. Th us, it is possible that some of the

patients in our analysis who apparently did not undergo screening

had, in fact, received a colonoscopy in the 5 years before the study

time frame. Th is explanation, however, would seem to pertain only

to those patients who received no FOBT during the study period

because FOBT is typically no longer indicated once colonoscopy is

chosen as the screening method.

Second, our analysis was not able to capture data on tests per-

formed outside of the VHA if not paid for by the VHA. Th is

limitation may have resulted in an underestimation of the ade-

quacy of screening, although it is unlikely that the 30 percent-

age point discrepancy between VHA performance measures and

our fi ndings could be explained solely by such missing data. In

fact, we found that veterans with outside insurance were more

likely to receive adequate screening, which is consistent with

previously reported fi ndings that dual eligible veterans receiving

care through the VHA are more likely to receive preventive care

( 26 ). Furthermore, rates of dual use in the VHA are reported to

be < 30 % ( 14,27 ). Even if 30 % of veterans in our sample under-

went adequate screening outside of the VHA at the rate equiva-

lent to that identifi ed in our study, the resulting proportion would

remain < 70 % .



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Table 3 . Longitudinal adherence to FOBT in men receiving FOBT alone a

Characteristic Receipt of FOBT out of 5 years (excludes those receiving endoscopy) Adjusted odds ratio b

(95 % CI)

1 2 3 ≥ 4

N ( % ) 161,863 (42.1 % ) 100,097 (26.0 % ) 68,371 (17.8 % ) 54,196 (14.1 % )

Age, years, mean (s.d.) 63.5 (8.0) 64.0 (7.8) 64.4 (7.6) 65.1 (7.4) 1.02 (1.02 – 1.02)


Non-Hispanic white 74,603 (40.2) 48,613 (26.2) 34,458 (18.6) 27,824 (15.0) Ref

Non-Hispanic black 13,158 (43.5) 8,072 (26.7) 5,223 (17.3) 3,793 (12.5) 0.87 (0.84 – 0.90)

Other c 11,082 (58.3) 4,747 (25.0) 2,019 (10.6) 1,145 (6.0) 0.46 (0.43 – 0.49)

Unknown 62,645 (42.0) 38,479 (25.8) 26,576 (17.8) 21,381 (14.3) 0.94 (0.92 – 0.96)


Married 102,479 (41.4) 64,470 (26.1) 44,144 (17.8) 36,246 (14.7) Ref

Other 57,193 (43.1) 34,495 (26.0) 23,447 (17.7) 17,486 (13.2) 0.95 (0.93 – 0.97)

Unknown 1,815 (47.1) 946 (24.5) 684 (17.7) 411 (10.7) 0.76 (0.69 – 0.85)


No 83,887 (43.5) 50,525 (26.2) 33,618 (17.4) 24,803 (12.9) Ref

Yes 77,593 (40.6) 49,381 (25.9) 34,654 (18.1) 29,338 (15.4) 1.07 (1.05 – 1.09)


No 71,295 (42.3) 44,061 (26.1) 29,975 (17.8) 23,380 (13.9) Ref

Yes 90,568 (42.0) 56,036 (26.0) 38,396 (17.8) 30,816 (14.3) 1.08 (1.06 – 1.10)


None 105,611 (42.1) 64,436 (25.7) 44,520 (17.7) 36,513 (14.5) Ref

SC < 50 % 35,054 (42.3) 22,074 (26.6) 14,697 (17.7) 11,043 (13.3) 0.94 (0.91 – 0.96)

SC > 50 % 19,370 (41.4) 12,588 (26.9) 8,551 (18.3) 6,244 (13.4) 0.99 (0.96 – 1.02)

AA / housebound d 1,453 (46.6) 813 (26.1) 508 (16.3) 343 (11.0) 0.77 (0.69 – 0.87)


0 82,198 (42.7) 49,775 (25.8) 33,813 (17.5) 26,917 (14.0) Ref

1 27,542 (41.0) 17,512 (26.1) 12,311 (18.3) 9,831 (14.6) 1.02 (0.997 – 1.05)

2 30,451 (41.5) 19,217 (26.2) 13,174 (17.9) 10,578 (14.4) 1.01 (0.99 – 1.04)

≥ 3 21,672 (42.3) 13,593 (26.5) 9,073 (17.7) 6,870 (13.4) 0.92 (0.89 – 0.95)

BMI, n ( % )

15 to < 18.5 1,283 (46.6) 734 (26.6) 434 (15.7) 305 (11.1) 0.80 (0.70 – 0.90)

18.5 to > 25 30,781 (42.2) 19,009 (26.0) 12,938 (17.7) 10,292 (14.1) Ref

25 to < 30 61,698 (40.8) 39,085 (25.8) 27,790 (18.4) 22,810 (15.1) 1.06 (1.03 – 1.09)

≥ 30 54,589 (41.8) 34,507 (26.4) 23,442 (17.9) 18,214 (13.9) 0.99 (0.96 – 1.02)

Region, n ( % )

South 65,088 (41.4) 41,251 (26.2) 28,173 (17.9) 22,825 (14.5) Ref

Northeast 28,833 (39.7) 18,274 (25.1) 13,644 (18.8) 11,950 (16.4) 1.08 (1.05 – 1.11)

Midwest 31,832 (45.1) 18,006 (25.5) 11,593 (16.4) 9,215 (13.0) 0.81 (0.79 – 0.83)

West 35,675 (43.0) 22,351 (26.9) 14,846 (17.9) 10,140 (12.2) 0.82 (0.80 – 0.84)

AA, aid and attendance; BMI, body mass index; CI, confi dence interval; FOBT, fecal occult blood test; SC, service connected; VA, Veterans Affairs. a Number of observations after case-wise deletion in adjusted logistic regression model=357,193; C-statistic for model=0.57. b Odds ratio refers to comparison of those receiving ≥ 4 FOBTs when compared with those receiving 1 – 3 FOBT(s). c Other (race) refers to Hispanic, Asian, and American Indian veterans. d AA and housebound benefi ts are available to veterans who have in-home care or who live in nursing homes or assisted living facilities.

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Table 4 . Longitudinal adherence to FOBT in women receiving FOBT alone a

Characteristic Receipt of FOBT out of 5 years (excludes those receiving endoscopy) Adjusted odds ratio b

(95 % CI)

1 2 3 ≥ 4

N ( % ) 4,492 (42.9) 2,732 (26.1) 1,815 (17.3) 1,430 (13.7)

Age, years, mean (s.d.) 59.8 (7.4) 60.0 (7.4) 60.0 (7.3) 60.7 (7.5) 1.02 (1.01 – 1.03)


Non-Hispanic white 2,404 (43.0) 1,404 (25.1) 971 (17.4) 811 (14.5) Ref

Non-Hispanic black 349 (40.8) 231 (27.0) 157 (18.4) 118 (13.8) 0.92 (0.74 – 1.14)

Other c 141 (46.8) 82 (27.2) 53 (17.6) 25 (8.3) 0.51 (0.32 – 0.82)

Unknown 1,596 (43.0) 1,012 (27.2) 631 (17.0) 475 (12.8) 0.89 (0.78 – 1.01)


Married 1,904 (43.6) 1,135 (26.0) 721 (16.5) 603 (13.8) Ref

Other 2,514 (42.4) 1,547 (26.1) 1,063 (17.9) 811 (13.7) 0.95 (0.84 – 1.07)

Unknown 72 (44.4) 47 (29.0) 28 (17.3) 15 (9.3) 0.72 (0.42 – 1.25)


No 2,298 (41.8) 1,453 (26.4) 987 (18.0) 757 (13.8) Ref

Yes 2,192 (44.1) 1,276 (25.7) 825 (16.6) 672 (13.5) 0.86 (0.76 – 0.97)


No 1,802 (42.5) 1,072 (25.3) 732 (17.3) 635 (15.0) Ref

Yes 2,690 (43.2) 1,660 (26.7) 1,083 (17.4) 795 (12.8) 0.85 (0.76 – 0.96)


None 3,199 (43.6) 1,932 (26.3) 1,230 (16.8) 972 (13.3) Ref

SC < 50 % 693 (41.8) 408 (24.6) 321 (19.4) 235 (14.2) 1.13 (0.96 – 1.33)

SC ≥ 50 % 563 (40.1) 372 (26.5) 249 (17.7) 219 (15.6) 1.31 (1.11 – 1.55)

AA / housebound d 35 (52.2) 17 (25.4) 12 (17.9) 3 (4.5) 0.33 (0.10 – 1.05)


0 2,699 (42.4) 1,640 (25.7) 1,116 (17.5) 918 (14.4) Ref

1 570 (44.0) 352 (27.2) 213 (16.4) 161 (12.4) 0.85 (0.71 – 1.03)

2 803 (42.3) 510 (26.9) 331 (17.4) 253 (13.3) 0.91 (0.78 – 1.06)

≥ 3 420 (46.5) 230 (25.5) 155 (17.2) 98 (10.9) 0.69 (0.54 – 0.86)

BMI, n ( % )

15 to < 18.5 63 (44.4) 35 (24.6) 28 (19.7) 16 (11.3) 0.72 (0.42 – 1.23)

18.5 to < 25 971 (42.7) 563 (24.8) 390 (17.2) 350 (15.4) Ref

25 to < 30 1,304 (42.0) 804 (25.9) 565 (18.2) 433 (13.9) 0.90 (0.77 – 1.05)

≥ 30 1,873 (43.0) 1,175 (27.0) 746 (17.1) 565 (13.0) 0.86 (0.74 – 0.99)

Region, n ( % )

South 1,865 (41.0) 1,149 (25.3) 815 (17.9) 718 (15.8) Ref

Northeast 577 (43.0) 320 (23.8) 230 (17.1) 216 (16.1) 1.02 (0.86 – 1.22)

Midwest 726 (45.3) 460 (28.7) 247 (15.4) 169 (10.5) 0.66 (0.55 – 0.79)

West 1,321 (44.6) 798 (26.9) 519 (17.5) 326 (11.0) 0.65 (0.56 – 0.75)

AA, aid and attendance; BMI, body mass index; CI, confi dence interval; FOBT, fecal occult blood test; SC, service connected; VA, Veterans Affairs. a Number of observations after case-wise deletion in adjusted logistic regression model=9,869; C-statistic for model=0.59. b Odds ratio refers to comparison of those receiving ≥ 4 FOBTs when compared with those receiving 1 – 3 FOBT(s). c Other (race) refers to Hispanic, Asian, and American Indian veterans. d AA and housebound benefi ts are available to veterans who have in-home care or who live in nursing homes or assisted living facilities.



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Study Highlights

WHAT IS CURRENT KNOWLEDGE 3 Fecal occult blood testing (FOBT) is a recommended

screening strategy for colorectal cancer.

3 Current quality measures for colorectal cancer screening do not assess adherence with repeated testing.

WHAT IS NEW HERE 3 Longitudinal adherence to guaiac FOBT is low.

3 Current colorectal cancer screening quality measures will overestimate the effectiveness of screening programs.

3 These fi ndings may similarly apply to immunochemical FOBT.

REFERENCES 1 . Jemal A , Siegel R , Ward E et al. Cancer statistics, 2009 . CA Cancer J Clin

2009 ; 59 : 225 – 49 . 2 . Gellad ZF , Provenzale D . Colorectal cancer: national and international

perspective on the burden of disease and public health impact . Gastroenter-ology 2010 ; 138 : 2177 – 90 .

3 . Levin B , Lieberman DA , McFarland B et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology . Gastroenterology 2008 ; 134 : 1570 – 95 .

4 . Hardcastle JD , Chamberlain JO , Robinson MH et al. Randomised control-led trial of faecal-occult-blood screening for colorectal cancer . Lancet 1996 ; 348 : 1472 – 7 .

5 . Kronborg O , Fenger C , Jorn O . Randomised study of screening for colorec-tal cancer with faecal-occult-blood test . Lancet 1996 ; 348 : 1467 – 71 .

6 . Mandel JS , Bond JH , Church TR . Reducing mortality from colorectal cancer by screening for fecal occult blood . N Engl J Med 1993 ; 328 : 1365 – 71 .

7 . Centers for Disease Control and Prevention (CDC) . Use of colorectal can-cer tests — United States, 2002, 2004, and 2006 . MMWR Morb Mortal Wkly Rep 2008 ; 57 : 253 – 8 .

8 . Schenck AP , Peacock SC , Klabunde CN et al. Trends in colorectal cancer test use in the Medicare population, 1998 – 2005 . Am J Prev Med 2009 ; 37 : 1 – 7 .

9 . El-Serag HB , Petersen L , Hampel H et al. Th e use of screening colonoscopy for patients cared for by the Department of Veterans Aff airs . Arch Intern Med 2006 ; 166 : 2202 – 8 .

10 . U.S. Preventive Services Task Force . Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement . Ann Intern Med 2008 ; 149 : 627 – 37 .

11 . Rex DK , Johnson DA , Anderson JC et al. American College of Gastroenter-ology Guidelines for Colorectal Cancer Screening 2008 . Am J Gastroenterol 2009 ; 104 : 739 – 50 .

12 . HEDIS 2010: Health Plan Employer Data and Information Set . National Committee for Quality Assurance: Washington, DC , 2010 . Accessed on 1 March 2010 at http://www.ncqa.org/tabid/1044/Default.aspx .

13 . VA Offi ce of Quality and Performance . FY 2010 VHA Performance Meas-urement System Technical Manual, 2010 ; available at: http://vaww.oqp.med.va.gov/programs/pm/performance.aspx ; accessed 31 January 2011 .

14 . Yancy WS , McDuffi e JR , Stechuchak KM et al. Obesity and receipt of clinical preventive services in veterans . Obesity 2010 ; 18 : 1827 – 35 .

15 . Zeber JE , Grazier KL , Valenstein M et al. Eff ect of a medication copayment increase in veterans with schizophrenia . Am J Manag Care 2007 ; 13 : 335 – 46 .

16 . Quan H , Sundararajan V , Halfon P et al. Coding algorithms for defi ning comorbidities in ICD-9-CM and ICD-10 administrative data . Med Care 2005 ; 43 : 1130 – 9 .

17 . Schneeweiss S , Wang PS , Avorn J et al. Improved comorbidity adjust-ment for predicting mortality in Medicare populations . Health Serv Res 2003 ; 38 : 1103 – 20 .

18 . Department of Veteran Aff airs Offi ce of Quality and Performance: Perform-ance Data Resource Center . Available at : http://vaww.oqp.med.va.gov/programs/pm/pmReports.aspx ; accessed 31 January 2011 .

Another potential limitation of our analysis is its dependence on

claims data. In general, claims data do not reliably allow diff eren-

tiation of tests performed for screening or nonscreening reasons

( 28 ). One exception is with FOBT within the VHA, where the reli-

ability of outpatient claims measurements for identifying FOBT

performed for screening purposes has been previously validated

( 29 ). Th e limitation may apply to the other CRC screening tests

(e.g., colonoscopy) but would apply equally to existing quality

measures in which screening and diagnostic procedures are not

diff erentiated.

In conclusion, our study highlights a potential weakness of

current performance measures for CRC screening, which assess

receipt of FOBT cross-sectionally even though the services are

performed repeatedly over a number of years. We suggest a change

of quality indicators from measuring rates of service receipt cross-

sectionally to measuring the rates of adequate screening longitu-

dinally. Assessment of adequate screening requires performance

measures to incorporate test indication ( 28 ) as well as adherence

with repeated testing. For CRC, and, by extension, for other clinical

preventive and disease management services, this goal will neces-

sitate new, standardized longitudinal measures of quality. Obtain-

ing longitudinal measures will require integrated electronic health

records where adherence patterns can be reliably assessed outside

of clinical trials and strategies for overcoming barriers to participa-

tion in national clinical data registries.

ACKNOWLEDGMENTS We thank Dr Eugene Oddone for his thoughtful comments on an

earlier version of the manuscript. Th e views expressed in this article

are those of the authors and do not necessarily refl ect the position

or policy of the Department of Veterans Aff airs or the United States

government.

CONFLICT OF INTEREST Guarantor of the article : Ziad F. Gellad, MD, MPH.

Specifi c author contributions : Study concept and design: Gellad,

Stechuchak, Fisher, Olsen, and Yancy; acquisition of data: Stechuchak,

Olsen, McDuffi e, and Yancy; analysis and interpretation of data:

Gellad, Stechuchak, Fisher, Olsen, Østbye, and Yancy; draft ing of the

manuscript: Gellad and Stechuchak; critical revision of the manuscript

for important intellectual content: Gellad, Stechuchak, Fisher, Olsen,

McDuffi e, Østbye, and Yancy; statistical analysis: Gellad, Stechuchak,

and Olsen; administrative, technical, or material support:

Gellad, Fisher, and Yancy; study supervision: Fisher and Yancy.

Financial support : Funding for the study was provided by the

Department of Veterans Aff airs (IIR-05-127). Dr Gellad is sup-

ported in part by a Career Development Award from the American

Society for Gastrointestinal Endoscopy. Dr Yancy was supported

by a VHA Health Services Research and Development grant (RCD

02-183-1) from the Department of Veterans Aff airs. Dr Fisher is

supported by a VA Career Development Transition Award (RCD

04-174). Th e funding source had no role in the design, conduct, or

analysis of this study or in the decision to submit the manuscript

for publication.

Potential competing interests : None.

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19 . Sonnenberg A , Delco F , Inadomi JM . Cost-eff ectiveness of colonoscopy in screening for colorectal cancer . Ann Intern Med 2000 ; 133 : 573 – 84 .

20 . Myers RE , Balshem AM , Wolf TA et al. Adherence to continuous screening for colorectal neoplasia . Med Care 1993 ; 31 : 508 – 19 .

21 . O ’ Malley AS , Forrest CB , Mandelblatt J . Adherence of low-income women to cancer screening recommendations . J Gen Intern Med 2002 ; 17 : 144 – 54 .

22 . Subramanian S , Klosterman M , Amonkar MM et al. Adherence with color-ectal cancer screening guidelines: a review . Prev Med 2004 ; 38 : 536 – 50 .

23 . Th omas W , White CM , Mah J et al. Longitudinal compliance with annual screening for fecal occult blood. Minnesota Colon Cancer Control Study . Am J Epidemiol 1995 ; 142 : 176 – 82 .

24 . Cooper GS , Koroukian SM . Geographic variation among Medicare ben-efi ciaries in the use of colorectal carcinoma screening procedures . Am J Gastroenterol 2004 ; 99 : 1544 – 50 .

25 . Ashton CM , Petersen NJ , Souchek J et al. Geographic variations in utilization rates in Veterans Aff airs hospitals and clinics . N Engl J Med 1999 ; 340 : 32 – 9 .

26 . Keyhani S , Ross JS , Hebert P et al. Use of preventive care by elderly male veterans receiving care through the Veterans Health Administration, Medicare fee-for-service, and Medicare HMO plans . Am J Public Health 2007 ; 97 : 2179 – 85 .

27 . Borowsky SJ , Cowper DC . Dual use of VA and non-VA primary care . J Gen Intern Med 1999 ; 14 : 274 – 80 .

28 . Walter LC , Davidowitz NP , Heineken PA et al. Pitfalls of converting prac-tice guidelines into quality measures: lessons learned from a VA perform-ance measure . JAMA 2004 ; 291 : 2466 – 70 .

29 . Fisher DA , Galanko J , Dudley TK et al. Impact of comorbidity on colorectal cancer screening in the veterans healthcare system . Clin Gastroenterol Hepatol 2007 ; 5 : 991 – 6 .

Documents

Longitudinal Adherence to Fecal Occult Blood Testing Impacts Colorectal Cancer Screening Quality