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The Impact of Practice Guidelines in the Management of Barrett Esophagus
A National Prospective Cohort Study of Physicians
Marcia Cruz-Correa, MD;
Cary P. Gross, MD;
Marcia Irene Canto, MD, MHS;
Michael Cabana, MD, MPH;
Richard E. Sampliner, MD;
J. Patrick Waring, MD;
Corlina McNeil-Solis, BS;
Neil R. Powe, MD, MPH, MBA
Arch Intern Med. 2001;161:2588-2595.
ABSTRACT
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Background Surveillance of patients with Barrett esophagus (BE) is recommended
to detect dysplasia and early cancer. In 1998, practice guidelines for the
surveillance of patients with BE were developed under the auspices of the
American College of Gastroenterology (ACG). Our objective is to assess physicians'
awareness of agreement with and adherence to these guidelines.
Methods A national prospective cohort study of practicing gastroenterologists
who completed a self-administered questionnaire containing case studies prior
to the release of the guidelines and another survey 18 months later. Analysis
of adherence to the guidelines was done using the McNemar  2
test.
Results Of the 154 gastroenterologists (66%) who responded to the follow-up
survey, more than half (55%) were aware of the guidelines, and members of
the ACG were more likely to know of their existence than nonmembers (61% vs
38%; P = .01). Overall, about 27% of physicians reported
practicing in accordance with the guidelines at baseline; adherence increased
modestly to 38% in the 18-month follow-up (P = .04)
and was inversely related to fee-for-service reimbursement. Awareness was
not associated with an increased likelihood of adherence, but agreement with
the guidelines was strongly correlated with adherence (P<.001). The most frequent reasons for disagreement were concerns
about liability, cancer risk, and inadequate evidence.
Conclusions Awareness of the guidelines published by the ACG was low. Guideline
awareness did not predict adherence. Improvement in guideline adherence will
require steps beyond mere dissemination and promotion. Addressing disagreements
about liability, disease risk, and scientific evidence as well as restructuring
payment incentives may help achieve optimal practice.
INTRODUCTION
SUCCESSFUL implementation of clinical practice guidelines should improve
quality of care by decreasing inappropriate variation.1-2
However, several studies have suggested that guidelines have limited impact
on clinical practice. These studies have examined neither prospectively the
continuum of guideline adoption from dissemination, to awareness, to agreement,
and finally to adherence nor the specific barriers along the way.
In 1998, practice guidelines for the surveillance of patients with Barrett
esophagus (BE) (columnar epithelium replacing normal squamous epithelium as
a consequence of gastroesophageal reflux disease) were developed under the
auspices of the American College of Gastroenterology (ACG),3
and drafts of the guidelines were submitted to 2 other professional associations,
the American Society for Gastrointestinal Endoscopy (ASGE) and the American
Gastroenterological Association (AGA), for their review and approval.3-4 Because of the well-known association
of BE with adenocarcinoma of the esophagus, regular endoscopic surveillance
with biopsy has been recommended to detect dysplasia and cancer at an early
stage.5-10
The ACG guidelines included specific surveillance intervals for BE with no
dysplasia, low-grade dysplasia, and high-grade dysplasia.
Adherence to guidelines such as these may depend on physicians' awareness
of them after dissemination and subsequent agreement. Identification of specific
barriers to physicians' adherence to guidelines will allow for the development
of interventions to improve adherence to guidelines and ultimately quality
of care. Therefore, we performed a national longitudinal study to assess the
impact of the ACG guidelines on physicians' decisions regarding surveillance
and management of patients with BE. In particular, we asked (1) Was publication
and awareness of the guidelines sufficient for adherence? (2) Did agreement
with the guideline's content promote adherence? (3) What factors were associated
with guideline adherence?
METHODS
STUDY DESIGN AND OVERVIEW
We conducted a national prospective cohort study (BE Surveillance and
Treatment) of practicing gastroenterologists using a self-administered questionnaire.
Physicians were eligible if they were members of the ACG, AGA, or ASGE and
were not in training programs. Physicians who were retired or did not perform
upper endoscopy were excluded. We used a stratified, random sampling method,
with stratification based on membership in 1 of 3 gastrointestinal organizations.
SURVEY DISTRIBUTION
The baseline survey was distributed between March and June 1998; this
was just prior to the publication of the BE guidelines in the American Journal of Gastroenterology.3
We distributed the baseline survey and letters ensuring anonymity to the 722
gastroenterologists in our sample; 88 people (12%) had incorrect addresses
and could not be contacted with directory assistance, while 79 others (11%)
indicated that they did not perform upper endoscopy regularly. Of the 555
eligible respondents, we received 279 completed surveys (response rate, 50.3%).
The follow-up survey was distributed to respondents of the baseline survey
18 months later between October 1999 and January 2000. We attempted to make
telephone contact with all individuals who had not responded to the 2 mailed
surveys. Finally, we mailed a third copy of the survey to individuals after
the telephone reminder.
CONTENT OF THE QUESTIONNAIRE
The baseline and follow-up surveys included 3 case scenarios involving
a patient with BE. This patient was described as
" . . . a 55 year-old white male with an eight-year history of
moderately severe reflux and no other prominent symptoms or medical history.
At endoscopy, he is found to have columnar-type epithelium in the distal esophagus
that extends proximally about ten centimeters. Biopsies confirm the presence
of specialized columnar epithelium."
In the first scenario, the pathological reading showed no dysplasia.
In the second and third scenarios, the biopsy results were consistent with
low-grade and high-grade dysplasia, respectively. Respondents were asked how
they would manage each patient with regard to frequency of endoscopic surveillance,
endoscopy technique, and surgical management.
The follow-up survey had 3 additional sections. First, to assess respondents'
awareness of the published guidelines for the management of BE, we asked whether
certain organizations had developed guidelines for the management of BE and
if those guidelines included specific endoscopic surveillance recommendations.
We included the organizations that have actually issued joint guidelines (the
ACG, AGA, and ASGE) along with other organizations (local provider, health
maintenance organization/local insurer, the Health Care Financing Administration,
and the Agency for Healthcare Research and Quality). Second, we asked physicians
whether they agreed, disagreed, or were undecided with 5 statements about
the recommended surveillance strategy for BE as described in the published
practice guidelines.3 The participants were
asked to select the rationale for their response from a list of numbered potential
reasons (medical, legal, economic, consumer, or scientific); perceived risk
of cancer; medicolegal threats; cost of surveillance; patient demand for surveillance;
published literature evidence; peer recommendations; and knowledge of guidelines.
Third, we asked respondents whether they agreed with the concept of clinical
practice guidelines and information about their demographic characteristics,
practice setting, and prior experience with BE.
STATISTICAL ANALYSIS
Our main outcomes were awareness of, agreement with, and adherence to
the guidelines. We calculated the proportion of respondents who were aware
of the guidelines and agreed with each of its specific recommendations. We
used 2 analysis and multiple logistic regression to identify
factors associated with awareness and agreement with the guidelines.
We examined the frequency of follow-up endoscopic surveillance for patients
with BE across various grades of dysplasia. We defined guideline adherence
as the frequency of endoscopic surveillance within 25% of that suggested by
the guidelines. The ACG guidelines recommend endoscopic surveillance every
24 to 36 months for BE with no dysplasia.3
For BE with low-grade dysplasia, the ACG guidelines recommend endoscopic surveillance
every 6 months during the first year and every 12 months thereafter.3 For BE with high-grade dysplasia, the guidelines recommend
endoscopic surveillance every 3 months or esophagectomy.3
We then identified the respondents who were guideline adherent for each specific
case scenario: no dysplasia, low-grade dysplasia, and high-grade dysplasia.
Overall compliance was defined as practice in accordance with the guidelines
in all 3 case scenarios: no dysplasia, low-grade dysplasia, and high-grade
dysplasia.
Guideline adherence was expressed as the percentage of respondents to
the baseline and follow-up surveys who were guideline adherent for each specific
grade of dysplasia as well as the grades overall. To compare the proportion
of respondents who were guideline adherent prior to the dissemination of the
guidelines with the proportion who were adherent 18 months later, we used
the McNemar 2test.11
We used multiple logistic regression to identify factors that were independently
associated with adherence to the guidelines. In addition, we performed multiple
logistic regression analysis to identify factors independently associated
with recommending esophagectomy for patients with high-grade dysplasia. A
bootstrapping technique was used to obtain the 95% confidence intervals and
SEs for the multiple logistic regression models.12
Variables for the final logistic regression model were selected by using both
stepwise- and hypothesis-driven procedures.13
Statistical analyses were performed using Stata 6.0 (Stata Corp, College Station,
Tex).
RESULTS
PHYSICIAN ELIGIBILITY, RESPONSE RATE, AND CHARACTERISTICS
We distributed 279 surveys; 44 people (16%) had incorrect addresses
and could not be contacted with directory assistance or membership directories.
Of the 235 eligible respondents who had completed the baseline survey, we
received 154 completed surveys (response rate, 66%). Respondents did not differ
from nonrespondents with regard to professional society membership, age, sex,
academic appointment, or years since completing fellowship training. The mean
age of respondents was 48.1 years; 93% were men (Table 1). Of the respondents, 56% had an appointment at an academic
medical center. Fee for service was the most common means of reimbursement,
followed by salary. About a quarter of the respondents had graduated from
gastroenterology training within 8 years of the baseline survey. Nearly half
of the respondents were members of all 3 societies (the ACG, AGA, and ASGE).
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Table 1. Characteristics of 154 Respondents
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AWARENESS OF THE GUIDELINES FOR MANAGEMENT AND SURVEILLANCE OF BE
Of the respondents, 85 (55%) reported that the ACG had issued guidelines
for the management of BE. Members of the ACG were more likely to be aware
of the guidelines than nonmembers (61.2% vs 37.5%; P
= .01). However, many respondents could not discriminate between the societies
regarding guideline authorship; 51 (33%) of our respondents reported that
all 3 societies have published guidelines for the management of BE. Additionally,
respondents who had completed their fellowship training most recently (within
8 years of the baseline survey [27% of the respondents]) were significantly
more likely to be aware of the guidelines than their more experienced counterparts
(68% vs 49%, respectively; P = .04).
MANAGEMENT OF PATIENTS AND ADHERENCE TO THE GUIDELINES
No Dysplasia
Table 2 gives the management
plans for the 3 case scenarios. For patients without dysplasia, most of the
respondents indicated that they would follow the patients with regular endoscopic
surveillance, with only less than 1% choosing no further action. This treatment
strategy was not significantly different from the strategy proposed at baseline
(P = .56). Two thirds (66%) of respondents recommended
an initial surveillance frequency with esophagogastroduodenoscopy every 7
to 12 months. If findings were unchanged after the initial surveillance, 70%
recommended that the follow-up interval be lengthened to 18 to 24 months.
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Table 2. Approach to Patients With Barrett Esophagus Before and After
Release of Clinical Practice Guidelines*
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Table 3 presents the frequencies
of adherence to the guidelines for BE management and surveillance in the baseline
and follow-up surveys. Compliance with practice guidelines for BE with no
dysplasia was observed in 81% of the respondents at follow-up, a 9.7 percentage
point increase from the baseline survey (P = .03).
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Table 3. Adherence to Recommendations for Management and Surveillance
of Barrett Esophagus by Gastroenterologists Before and After Release of Clinical
Practice Guidelines*
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Low-grade Dysplasia
For patients with BE having low-grade dysplasia, nearly our entire sample
of physicians indicated that they would perform regular endoscopic surveillance
on both the baseline and follow-up surveys. Table 2 demonstrates that the recommended interval for surveillance
with esophagogastroduodenoscopy was shorter for these patients than for those
without dysplasia, as 86% of the respondents selected an interval of 6 or
fewer months in the follow-up survey. For subsequent surveillance, 56% of
the respondents would perform another endoscopy between 7 and 12 months. In
the baseline survey, about 36% of the respondents were practicing in concordance
with the guideline recommendations; although the percentage increased slightly
in the follow-up survey, it was not statistically significant (Table 3).
High-grade Dysplasia.
For patients with high-grade dysplasia, approximately three quarters
of the respondents recommended esophagectomy, and a fourth recommended endoscopic
surveillance on both the baseline and follow-up surveys. Among those who recommended
surveillance, the most common surveillance interval in both surveys was 3
months or less, as was selected by 73% and 70% of the respondents in the baseline
and follow-up surveys, respectively (Table
2). Hence, in the case of high-grade dysplasia, most of the respondents
to both surveys were practicing in accordance with the guidelines (Table 3).
Overall Adherence
Of the respondents, 38% were practicing in accordance with the guidelines
in the follow-up survey. This represents an increase of almost 11 percentage
points in guideline compliance between the baseline and follow-up surveys
(Table 3).
PHYSICIAN CHARACTERISTICS ASSOCIATED WITH GUIDELINE ADHERENCE
We evaluated factors that were independently associated with guideline
adherence in a multivariate analysis (Table
4). For overall adherence (all 3 grades), physicians who were reimbursed
mainly on a fee-for-service basis performed more frequent endoscopic surveillance
and had an 84% lower odds of adhering to the guidelines than their counterparts
reimbursed on a salary or capitated basis (odds ratio [OR], 0.16; P = .002). As the percentage of fee-for-service reimbursement increased,
adherence to the guidelines decreased (Figure
1).
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Table 4. Relation Between Physician Characteristics and Management
of Barrett Esophagus After Release of Clinical Practice Guidelines
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Relationship of physicians' adherence to guidelines for management
of Barrett esophagus to reimbursement on a fee-for-service basis (2 for the trend, 6.51; P = .01).
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For the management of BE with no dysplasia, none of the physician characteristics
was independently associated with adherence. In the multivariate model for
low-grade dysplasia, physicians who were reimbursed mainly on a fee-for-service
basis had a 76% lower odds of adhering to the guidelines than their counterparts
(OR, 0.24; P = .01).
Respondents who reported that the ACG had issued guidelines for the
management of BE were less likely to comply with the guidelines for BE with
low-grade dysplasia (OR, 0.25; P = .01). Respondents
who reported that the ASGE had guidelines for the management of BE were more
likely to recommend esophagectomy for high-grade dysplasia (OR, 7.4; P = .002). Sex, academic appointment, society membership,
and the number of years since completing training were all unrelated to adherence
to any of the guidelines for BE.
AGREEMENT WITH THE GUIDELINES AMONG ADHERENTS AND NONADHERENTS
Table 5 presents the distribution
of respondents' agreement with guideline recommendations for each degree of
dysplasia. More than 80% of the respondents agreed with the recommendations
for the management of patients with either no dysplasia or high-grade dysplasia.
However, for the management of patients with low-grade dysplasia, only 63%
of the respondents agreed with the recommendations.
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Table 5. Adherence to American College of Gastroenterology Guidelines
According to Agreement vs Disagreement With Guideline Recommendation
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Respondents who agreed with the guidelines for management of BE for
no dysplasia and low-grade dysplasia were more than 10 times more likely to
adhere to the guidelines on the case scenarios than the respondents who disagreed
with the guidelines (P<.001). Similarly, respondents
who agreed with esophagectomy were more likely to recommend esophagectomy
(OR, 14.7; P<.001) than their counterparts.
REASONS FOR GUIDELINE AGREEMENT OR DISAGREEMENT
Table 6 presents the reasons
for agreement or disagreement with the published guidelines for the management
of BE in a multiple logistic regression model adjusted for the other reasons.
For BE with no dysplasia, the most common reasons for agreeing with the guidelines
were low-risk of cancer (P<.001) and adherence
to gastrointestinal society guidelines (P = .008).
Those respondents who disagreed with the guidelines were concerned about medicolegal
liability (P<.001) and the lack of published evidence
that supported this surveillance interval (P = .01).
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Table 6. Reasons for Agreement or Disagreement With the Specific Guidelines
by Dysplasia Grade on Management and Surveillance of Barrett Esophagus (BE)*
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For BE with low-grade dysplasia, the perceived risk of cancer was given
as the main reason both for agreement or disagreement with the guidelines
(P<.001), while adherence to gastrointestinal
society guidelines was independently associated with agreement (P<.001). For BE with high-grade dysplasia, the most common reasons
for agreeing with treatment with esophagectomy were (1) adequate published
literature that supports the surveillance strategy (P
= .005), (2) high risk of cancer associated with this histological stage (P<.001), and (3) concern about medicolegal liability
(P = .04).
Of our respondents, 139 (91%) agreed with the concept of clinical practice
guidelines. Among those who disagreed with guidelines, 10 (71%) reported that
guidelines were too rigid to apply to their practice (too "cookbook"). Only
2 of our respondents reported lack of confidence in guideline developers.
COMMENT
Despite wide promulgation, guidelines have had a limited effect on changing
physician behavior.14 Prior studies have lacked
a design that would allow evaluation of the continuum of guideline adoption
from dissemination, to awareness, to agreement, and finally, to adherence.15-21
To our knowledge, all have been either retrospective or cross-sectional studies.
We, however, prospectively examined the impact of practice guidelines on a
cohort of gastroenterologists before and after the publication of the guidelines
by the ACG. Furthermore, the present study design enabled us to document awareness
of and agreement with the guidelines as well as reasons associated with agreement
and disagreement.
In spite of publication of the ACG guidelines in the American Journal of Gastroenterology and ample citation of the guidelines
in other articles,22-25
only 55% of all respondents in our sample were aware of the guidelines 18
months after their publication. Although ACG members were more likely to be
aware than nonmembers, only 61% of the former group knew of the guidelines
despite uniform distribution of the journal to all society members.3 Physicians who completed their fellowship within 8
years of the publication of the guidelines were also more likely to be aware
of their existence.
The percentage of respondents who reported practicing in a manner suggested
by the guidelines increased from 27% (prior to the publication of the guidelines)
to 38% in the follow-up survey. Although this change was statistically significant,
it is not possible to determine whether the guidelines actually had an impact
on physician behavior because we did not directly evaluate individual physician
practices. There was wide disparity in the degree of guideline adherence when
the grade of dysplasia was considered. For the management of patients with
low-grade dysplasia, the percentage of respondents who were adherent with
the guidelines recommendations was low (43%). In contrast, more than 80% of
respondents were in compliance with published guidelines for BE with no dysplasia
and BE with high-grade dysplasia. These differences might result from the
lack of understanding of the natural history of BE (particularly of low-grade
dysplasia).26-27
Despite the significant change in overall adherence to the ACG guidelines,
awareness of the guidelines was not associated with increased adherence in
our study. Indeed, the 2 groups that were more likely to be aware of the guidelines
(ACG members and younger physicians) were not more likely to be practicing
in a manner consistent with the guidelines. The lack of association between
guideline awareness and adherence in our study is consistent with a prior
study that evaluated the impact of guideline publication on physician practice.28 The investigators reported that 78% of physicians
were aware of the guidelines, but only 26% of them changed their practices
to adhere to the new guidelines.28 It is clear
that guideline awareness does not guarantee change in practice behavior.
In our study, agreement with the ACG recommendations was strongly associated
with adherence. The most common reasons given for agreement with the guidelines
were (1) perceived risk of cancer in BE patients, (2) adherence to gastrointestinal
society guidelines, and (3) supportive published literature. Interestingly,
the most common reasons given for disagreement with the guidelines were (1)
perceived risk of cancer, (2) concerns about medical liability, and (3) lack
of published literature. Hence, the same body of existing data about the natural
history and treatment of BE has been interpreted in very different ways by
physicians; this has led to substantial practice variation. The risk of cancer
in BE has been estimated to be high29-30
in older studies and low in more recent ones.31
This may account for the increased likelihood of older physicians performing
more frequent surveillance for BE without dysplasia32
or recommending esophagectomy for BE with high-grade dysplasia, as shown in
our study. Variability in the estimation of cancer risk in BE may also influence
guideline adherence by American physicians because of concern for missing
malignancy diagnosis and the associated legal consequences. On the other hand,
in other health care systems, such as in the United Kingdom, the lack of evidence
on the efficacy of BE surveillance seems to be the most important factor influencing
BE management.27 Furthermore, there is no definitive
trial that proves the effectiveness of endoscopic surveillance for detecting
cancer in BE. There is also no study that compares various surveillance intervals
for the management of BE according to various grades of dysplasia.
We identified an inverse relationship between adherence to the guidelines
and fee-for-service reimbursement. Respondents who received most of their
reimbursement on a fee-for-service basis were less likely to adhere to the
guidelines primarily because they were more likely to recommend more frequent
endoscopy than that suggested by the guidelines. Fee-for-service reimbursement
has also been previously associated with more frequent surveillance for BE.33 This implies that restructuring payment incentives
may influence guideline adherence. When reimbursement is not linked to individual
services rendered, such as in countries in which many physicians are salaried,
the effectiveness of endoscopic surveillance may become a more important factor
that will influence physician practice.27
How can we improve adherence to practice guidelines? The first barrier
is lack of awareness.19 Professional societies
can play a major role in improving the quality of care through the creation
and dissemination of practice guidelines.34-35
The awareness rate of 61% among ACG members vs 38% among nonmembers in our
study suggests that the dissemination of the guidelines to society members
was relatively ineffective; additional strategies will be needed to reach
all members and nonmembers. Direct mailing may also be effective in improving
physician awareness, such as that performed by the National Institutes of
Health for its consensus statement on osteoporosis.36
The use of clinical alerts may also be helpful in disseminating new information
and changing physician practice.32 Guideline
dissemination via pharmaceutical representatives may also increase awareness,
but physicians may view the information from such sources with suspicion.37
The second barrier to physician adherence to guidelines is disagreement
with the specific recommendations. Increasing agreement with guideline recommendations
may be possible with interventions that target opinion leaders who may help
shape local consensus.38-39 Medical
communities can be relatively closed systems where changes in an individual's
practice are primarily influenced by colleagues and the norms and relationships
of local practice.40-41 When there
is practice variability because of lack of scientific evidence, performance
of well-designed studies with conclusive results may be more influential to
practicing physicians than expert opinions or guidelines. Future interventions
to change physician behavior should specifically address the reasons for disagreement
with guidelines, such as perceived risk of disease, patient demand, and medicolegal
liability. The construction and dissemination of guidelines should be an iterative
process, incorporating the concerns of practicing clinicians as well as patients.
This study has several limitations. First, the follow-up survey was
given to the respondents of our initial survey,33
which constituted 50% of the original eligible list of gastroenterologists.
In the follow-up survey, we obtained a response rate of 66%. Therefore, we
could have started with a select group of respondents. Our nonrespondents
were not significantly different from respondents with regard to age, sex,
professional society membership, and academic appointment. However, there
could be other important differences between respondents and nonrespondents
that remain unmeasured. Second, this was a self-reported survey, and respondents
might have selected answers they perceived to be correct. Finally, we sent
the follow-up survey 18 months after the guidelines for BE were published,
a relatively short period to fully assess the impact of the guidelines. Despite
this, we were able to document changes in physicians' approach.
CONCLUSIONS
Our longitudinal study demonstrated that after guideline publication
there was a significant increase in the proportion of respondents who reported
using the ACG-recommended BE surveillance protocol. However, the overall guideline
adherence rate was low, and lack of awareness did not seem to be the primary
barrier. Similarly, society membership did not predict adherence. The strongest
positive predictor of guideline adherence was agreement with the specific
recommendations, while the only negative predictor was predominantly fee-for-service
reimbursement. Hence, addressing specific practitioner concerns and reimbursement
incentives may increase adherence to clinical guidelines. In addition, identifying
the specific type of evidence that practitioners would find most useful could
facilitate the design of highly relevant studies, which may increase agreement
and adherence.
AUTHOR INFORMATION
Accepted for publication April 9, 2001.
This study was supported by training grant 2T32 DK07632-11 from the
National Institutes of Health, Bethesda, Md, an unrestricted grant from Janssen
Pharmaceutica Inc, Titusville, NJ, and the Robert Wood Johnson Clinical Scholars
Program, Princeton, NJ. Dr Powe is supported by grant K24DK02643 from the
National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda.
Corresponding author and reprints: Marcia Cruz-Correa MD, The Johns
Hopkins Hospital, Blalock 413, 600 N Wolfe St, Baltimore, MD 21287 (e-mail: macruzco{at}jhsph.edu).
From the Division of Gastroenterology-Hepatology (Drs Cruz-Correa and
Canto and Ms McNeil-Solis) and the Welch Center for Prevention, Epidemiology,
and Clinical Research (Dr Powe), Johns Hopkins University School of Medicine,
Baltimore, Md; Yale University School of Medicine, New Haven, Conn (Dr Gross);
the Department of Pediatrics, University of Michigan, Ann Arbor (Dr Cabana);
the Division of Gastroenterology, Tucson Veterans Affairs Medical Center and
University of Arizona Health Sciences Center, Tucson (Dr Sampliner); and the
Division of Gastroenterology, Emory University School of Medicine, Atlanta,
Ga (Dr Waring).
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