Abstract
Background
Although the prevalence of celiac disease in the USA approaches 1%, most cases are undiagnosed, in part, because of low adherence to the recommendation of submitting at least four specimens during duodenal biopsy. We aimed to determine whether physician and practice characteristics are associated with adherence to this recommendation.
Materials and methods
We used a large national pathology database to identify all adult patients who underwent duodenal biopsy during 2006–2009. Hierarchical modeling was used to determine whether procedure volume, the number of gastroenterologists per endoscopy suite, and the number of gastroenterologists per capita of the zip code of the practice were associated with adherence.
Results
We identified 92 580 patients (67% female, mean age 53.5 years) who met our inclusion/exclusion criteria. Specimens were submitted by 669 gastroenterologists from 200 endoscopy suites, located in 191 zip codes, with a mean of 3.4 gastroenterologists per suite. On multivariate analysis, a higher procedure volume was associated with a decreased adherence [odds ratio (OR) for each additional 100 procedures, 0.92; 95% confidence interval (CI), 0.88–0.97; P = 0.002]. An increased adherence was reported for gastroenterologists working at suites with higher numbers of gastroenterologists (OR for each additional gastroenterologist, 1.08; 95% CI, 1.04–1.13; P < 0.001) but not for a higher gastroenterologist density in the zip code of the practice (OR for each additional gastroenterologist per capita, 1.01; 95% CI, 0.99–1.03; P = 0.21).
Conclusion
High-volume physicians exhibit lower rates of adherence to biopsy guidelines, possibly because of the additional time required to submit at least four specimens. In contrast, a greater number of endoscopists working in an endoscopy suite are associated with an increased adherence, possibly because of peer education.
Keywords: celiac disease, endoscopy, quality of healthcare
Introduction
Celiac disease (CD) is common, with a population prevalence of 0.8–1% in the USA [1,2], which appears to be rising [3,4]. The majority of patients with CD in the USA remain undiagnosed [2,4,5]. CD is effectively treated with a gluten-free diet, and undiagnosed patients remain untreated. In the USA, the mean duration of symptoms before diagnosis and treatment is 11 years [6].
The diagnosis of CD is made by biopsy of the duodenum during upper gastrointestinal endoscopy and factors related to the performance of the duodenal biopsy may be contributing to the underdiagnosis of CD. Because the pathological abnormalities in CD can be patchy in the small intestine, guidelines from the American Gastroenterological Association issued in 2006 state that 4–6 specimens should be submitted when the diagnosis of CD is under consideration [7]. This recommendation was subsequently supported with data showing that the sensitivity of duodenal biopsy declines when fewer than four specimens are submitted [8] and that the diagnostic yield for CD increases with increasing specimen numbers [9].
Adherence to these guidelines in the USA is low. In a recent analysis of a national pathology database spanning the years 2006–2009, the most common number of specimens submitted during duodenal biopsy was two, and adherence to the standard of submitting at least four specimens occurred in only 35% of all duodenal biopsies [9]. In that study, even in procedures in which the indication field described a suspicion for CD, adherence to this standard only occurred in 38.5% of cases.
The 35% adherence rate was not evenly distributed among gastroenterologists [9]. There were a small number of providers who adhered to this standard more than 90% of the time, whereas there were a larger number of physicians whose adherence rate was less than 10%. This led us to question whether a physician’s practice milieu might affect adherence to this standard.
We aimed to determine whether physician and practice characteristics are associated with adherence to the recommendation to submit four or more specimens during duodenal biopsy.
In particular, in this study we examined whether the individual provider’s procedure volume influences adherence and whether proximity to other gastroenterologists influences adherence. We hypothesized that a high procedure volume and isolation from other gastroenterologists is associated with a decreased adherence. Proximity was measured separately as the number of gastroenterologists using the same endoscopy suite and as the number of gastroenterologists per capita in the zip code of the endoscopy suite.
Materials and methods
Miraca Life Sciences (formerly Caris Life Sciences) receives biopsy specimens from ambulatory surgical centers operating in 43 states, the District of Columbia, and Puerto Rico. Pathologists at Miraca Life Sciences make use of a uniform terminology and a database includes queriable findings.
For this study, we included adults, 18 years of age and older, who underwent a small intestinal biopsy during the years 2006 through 2009. Because this analysis focused on provider characteristics, and because we sought to measure changes in adherence over time, we included only examinations carried out by providers who performed endoscopy during at least 3 of these 4 years. For repeat endoscopies on the same patient, we included the first examination chronologically only.
Because this standard of submitting at least four specimens was recommended to increase the sensitivity for making a new diagnosis, we excluded any examinations performed on patients with a prior diagnosis of CD [7].
The primary outcome of interest was the submission of four or more specimens during duodenal biopsy. Covariates included in this analysis were age, sex, and year of the procedure. Physician variables included procedure volume, defined by the number of endoscopies with duodenal biopsy performed during this period, the number of physicians in each endoscopy suite who submitted samples to Miraca, and the regional physician density, defined by the number of gastroenterologists per capita in the zip code of each endoscopy suite. In addition, US Census data were used to measure the racial composition of the zip code of each endoscopy suite (percent black residents and percent Hispanic residents), the socioeconomic status of the endoscopy suite zip code (median household income and percent of population living in poverty), and the population density of the endoscopy suite zip code. A commercially available business listing database, the ReferenceUSA Healthcare database, was used to identify gastroenterologists practicing within the endoscopy suite zip code.
Statistical analysis
The submission of four or more specimens during duodenal biopsy was used to classify patients as having undergone a procedure that was congruent with the guidelines. We used the χ2-test to access the univariate associations between predictor variables and whether a patient had at least four specimens submitted. We used hierarchical linear modeling (using HLM 6; Scientific Software International, Skokie, Illinois, USA) to calculate multivariate adjusted odds ratios (ORs) for patients receiving a procedure that met the guidelines [10]. The HLM model included three levels: patients (level 1), nested within physicians (level 2), and physicians nested within endoscopy suites (level 3). Level 1 variables included patient age, sex, and the year of the procedure. Level 2 variables included physician volume over the study period. Level 3 variables included the number of endoscopists in the practice, the number of gastroenterologists per capita registered as practicing in the zip code of the study physician’s practice, the proportion of residents of the zip code who were black, Hispanic, and had an income below the poverty level, the median household income of the zip code, and the population density of the zip code.
The data were deidentified by Miraca Life Sciences before being provided to the investigators. The Institutional Review Board of Columbia University Medical Center evaluated this study protocol and deemed it as a ‘nonhuman subject research’ because of the deidentified nature of the data.
Results
During the 4-year period spanning between 2006 and 2009, duodenal biopsies from 150 155 patients were submitted. Of these 150 155 patients, 17 803 (12%) were excluded because of either a previous diagnosis of CD, a repeat procedure on the same patient, or a lack of information on the number of specimens submitted. An additional 39 772 patients (26%) were excluded because they were operated upon by physicians who did not perform the endoscopy in at least 3 years of the 4-year period. The remaining 92 580 patients were included in this analysis (Fig. 1).
Fig. 1.
Flowchart of adherence analysis. CD, celiac disease.
Characteristics of the patients and endoscopists are listed in Table 1. The mean patient age was 53.5 years, and 67% of the patients were female. There were 669 endoscopists, and the mean number of procedures with duodenal biopsy over the 4-year period was 138. There were 200 endoscopy suites in 191 zip codes, and a mean of 3.4 endoscopists per suite. The median number of gastroenterologists per 10 000 residents in the zip code of the study physician’s practice was 2.1 and in the highest quartile it was 6.2.
Table 1.
Characteristics of patients and practice settings
| Characteristics | N (%) |
|---|---|
| Patient age (mean/median±SD) | 53.5/54±16.8 |
| Patient sex | |
| Male | 30700 (33) |
| Female | 61 880 (67) |
| Year | |
| 2006 | 13 334 (34) |
| 2007 | 21 249 (32) |
| 2008 | 29711 (34) |
| 2009 | 28 286 (38) |
| Gastroenterologists | 669 |
| Procedure volume (mean/median±SD) | 138/88±168 |
| Endoscopy suites | 200 |
| Number of gastroenterologists per suite per year (mean/median±SD) | 3.4/2.8±2.5 |
| Number of gastroenterologists in zip code per 10 000 residents (mean/median±SD) | 3.5/2.1±6.7 |
In the univariate analyses, adherence to the standard of submitting at least four specimens occurred only in 35% of all patients (Table 2). An increasing patient age was associated with a decreased adherence, as was male sex. The adherence increased modestly over time, rising to 38% in 2009. The endoscopist’s procedure volume was associated with adherence. Biopsies performed by endoscopists in the lowest volume quartile had the highest adherence rate, 43%, whereas those performed by endoscopists in the highest volume quartile had the lowest adherence rate, 32% (P<0.001, Fig. 2). Biopsies performed by those practicing at endoscopy suites with five or more gastroenterologists had higher rates of adherence (40%), as compared with those at suites with the fewest gastroenterologists per suite (28%, P<0.0001). In contrast, proximity to other gastroenterologists by zip code did not affect adherence. Those physicians practicing in zip codes of low physician density (a mean of 0.52 gastroenterologists per 10 000) had similar adherence rates compared with those practicing in areas of higher density.
Table 2.
Association of patients and procedure settings with adherence to the recommendation to submit at least four specimens during duodenal biopsy
| Characteristics | Adherence (%) | P value |
|---|---|---|
| Patient age quartile | < 0.0001 | |
| 18–41 | 8726/22 872 (38) | |
| 42–53 | 8354/23 248 (36) | |
| 54–65 | 7299/21 919 (33) | |
| > 65 | 7611/24 541 (31) | |
| Patient sex | < 0.0001 | |
| Male | 10 239/30700 (33) | |
| Female | 21751/61 880 (35) | |
| Year | < 0.0001 | |
| 2006 | 4564/13 334 (34) | |
| 2007 | 6754/21 249 (32) | |
| 2008 | 10 057/29711 (34) | |
| 2009 | 10 615/28 286 (38) | |
| Gastroenterologists | ||
| Procedure volume quartile | < 0.0001 | |
| 3–40 | 1431/3366 (43) | |
| 41–87 | 3876/10 237 (38) | |
| 88–172 | 8273/21 450 (39) | |
| ≥173 | 18 410/57 527 (32) | |
| Number of gastroenterologists per suite | < 0.0001 | |
| 1–2 | 5768/20 674 (28) | |
| 3–4 | 6465/21 960 (29) | |
| ≥ 5 | 19757/49 946 (40) | |
| Number of gastroenterologists per 10 000 residents | < 0.0001 | |
| Quartile 1 (median 0.5) | 5705/15 438 (37) | |
| Quartile 2 (median 1.4) | 6422/18 671 (34) | |
| Quartile 3 (median 2.8) | 10 403/31 505 (33) | |
| Quartile 4 (median 6.2) | 9460/26 966 (35) |
Fig. 2.
Lower adherence to biopsy standards among higher volume providers.
The results of the multivariable hierarchical linear modeling are shown in Table 3. In the multivariate model, an older patient age and male sex remained independently associated with a decreased likelihood of submitting four or more specimens. An increasing endoscopy volume was associated with a decreased adherence to this recommendation [OR for each additional 100 procedures, 0.92; 95% confidence interval (CI), 0.88–0.97]. In contrast, an increase in the number of gastroenterologists at endoscopy suites was associated with an increased adherence, with each additional gastroenterologist present at the suite adding an 8% increase in the odds that a patient would have four or more specimens submitted (OR, 1.08; 95% CI, 1.04–1.13). The gastroenterologist density, defined by the number of gastroenterologists per capita in the zip code region, did not influence the odds of adherence (OR, 1.01; 95% CI, 0.99–1.03). The results presented here also adjust for the zip code level proportion of residents who were black and for population density. Further adjustment for zip code level median household income, percentage of the population living in poverty, and percentage of the population that was Hispanic did not alter the results.
Table 3.
Multivariable analysisa of factors independently associated with adherence
| Characteristics | Odds ratio |
95% CI | P value |
|---|---|---|---|
| Patient age (per 10 years) | 0.93 | 0.92–0.94 | < 0.001 |
| Sex | |||
| Male | 0.96 | 0.93–0.99 | 0.01 |
| Female | 1.0 | [reference] | |
| Gastroenterologist volume (per 100 procedures) | 0.92 | 0.88–0.97 | 0.002 |
| Suite (each additional gastroenterologist) | 1.08 | 1.04–1.13 | < 0.001 |
| Density (each additional gastroenterologist per 10 000 residents) | 1.01 | 0.99–1.03 | 0.21 |
CI, confidence interval.
Model includes year, racial composition of zip, population density of zip, and all variables in the table.
Discussion
In this analysis of 92 580 patients undergoing endoscopy with duodenal biopsy, we examined physician characteristics that influenced whether the recommended number of specimens was submitted. Patients undergoing biopsy by a high-volume gastroenterologist were less likely to have the recommended number of specimens submitted (32%) as compared with those undergoing biopsy by a low-volume gastroenterologist (43%, P<0.0001). Independently of this phenomenon, adherence to these recommendations was more common when biopsy was performed at a suite with five or more participating gastroenterologists (40%) as compared with a suite with one or two gastroenterologists (28%, P<0.0001).
The underdiagnosis of CD in the USA likely has a multifactorial etiology. It is unlikely that patients are less symptomatic than their European counterparts, as a multicenter case-finding initiative in the USA resulted in a dramatic (> 40-fold) increase in diagnosis rates among patients with a variety of signs and symptoms such as abdominal pain, diarrhea, and anemia [11]. Misinterpretation of the duodenal histology as normal may play a role in the failure to diagnose patients with subtle histological abnormalities [12]. Factors related to the performance of upper gastrointestinal endoscopy and biopsy have also been implicated in the underdiagnosis of CD. Among patients undergoing endoscopy for anemia, iron deficiency, diarrhea, or weight loss, in the majority of cases a duodenal biopsy is not performed [13,14]. When biopsy is performed, our previous study has shown that the recommended number of specimens is submitted in only 35% of all cases, despite a large incremental yield for diagnosing CD [9]. Given these low rates of adherence, and the variability of adherence rates between gastroenterologists, we sought to identify practice settings that are more or less conducive of adherence.
In this study, we found that high-volume gastroenterologists were less likely to adhere to the standard of submitting at least four specimens during duodenal biopsy. The procedure volume in gastrointestinal disease has been previously investigated in the context of cholecystectomy and Whipple procedures, for which a higher procedure volume was associated with improved outcomes [15,16]. In the field of gastrointestinal endoscopy, a higher hospital procedure volume is associated with decreased complication rates among patients undergoing endoscopic retrograde cholangiopancreatography [17].
The above associations between procedure volume and outcome are likely owed to the procedure complexity and the need for a certain volume to achieve or maintain particular skills. However, the procedure volume may impact outcomes in less complex tasks (such as the performance of duodenal biopsy during endoscopy) by means of other mechanisms. Studies on individual endoscopists’ procedure volume in gastroenterology are limited to colonoscopy. Although colonoscopies by high-volume providers have a higher successful completion rate [18], they may also have a lower rate of polyp identification and removal [19], possibly owing to fatigue during afternoon procedures [20]. The significance of this effect is unclear, as two studies have found no association between high-volume endoscopists and incidences of colorectal cancer after screening colonoscopy [21,22]. The mechanism of this association between procedure volume and low adherence is unknown. Perhaps high-volume endoscopists are less likely to adhere to this standard because of the additional time it would take to submit four or more specimens, adding approximately one additional minute to the procedure. A high-volume physician may believe that the incremental benefit of adherence is too small to justify spending this additional time, multiplied several times in a full schedule. However, without querying the knowledge and attitudes of these providers, this remains a matter of conjecture.
The impact of physician density on the quality of healthcare delivery has been extensively studied [23]. Regions with higher numbers of physicians per capita result in increased use of diagnostic tests and expenditures, without a clear impact on the quality of care [24]. In contrast, an increased density may lead to improved healthcare access, which may account for a lower incidence of late-stage presentations of colorectal cancer [25]. There is also evidence that outcomes in inflammatory bowel disease may be superior in areas with a high gastroenterologist density [26].
Although these studies focus principally on access to medical care and early intervention, another beneficial consequence of higher density may be the access to education from one’s peers on practice standards. Such an effect, if present, would be operative only if physicians were frequently in close proximity, such as in an endoscopy suite. Regions (as reflected by zip codes) of high physician density would not be expected to result in peer education if individual providers were practicing in separate (and possibly competing) locations. Congruent with this theory, we found that the adherence rates were higher in endoscopy suites that had high numbers of gastroenterologists but that adherence was not independently affected by the per capita density of gastroenterologists in the zip code where the study physician practiced. A complementary theory that may explain the increased adherence in suites with more gastroenterologists is that behavior is affected when the operator knows that others may be watching. Evidence supporting this concept is a study demonstrating that trainee involvement is associated with increased adenoma detection rates [27], and video-recording of colonoscopy is associated with a more careful withdrawal technique and, in some cases, improved adenoma detection [28,29].
The limitations of this study include a lack of clinical details in the database in terms of the underlying risk of CD in individual patients, such as serological information and a family history of CD. Further, physician characteristics such as age and years in practice, which may be associated with procedure volume and adherence, were not available. The size of the specimens and type of biopsy forceps used (e.g. large capacity vs. jumbo forceps) was not noted, though forceps size does not affect the sensitivity for detecting CD [30]. The measurement of physician volume was imperfect: it was limited to the database of duodenal biopsies and thus did not take into account upper endoscopies by providers who performed no biopsies or performed only gastric or esophageal biopsies, for example. It did not include a primary driver of procedure volume among gastroenterologists, colonoscopy. Moreover, it did not account for the fact that some providers perform additional endoscopies in settings that did not use this commercial pathology service. However, a misclassification of the provider volume due to this missing information would bias these results toward null. The fact that we still found an inverse relationship between provider volume and adherence indicates that this association is strong.
Conclusion
We found that high-volume physicians exhibit lower levels of adherence to biopsy recommendations. This may be a function of increased time pressure for these endoscopists, though the explanation is uncertain. A higher gastroenterologist density within endoscopy suites, but not within zip codes of practice, is associated with an increased adherence. This may be because of peer education or peer pressure with regard to practice standards. Efforts should be made to identify and promote settings conducive to adherence so as to maximize the quality of care delivered to patients undergoing endoscopy and in turn diagnose and treat symptomatic patients with CD.
Acknowledgements
Study concept and design: B.L., A.R., A.I.N., R.M.G., R.C.K., and P.H.G. Acquisition of data: B.L., R.M.G., D.S., and N.S.L. Analysis and interpretation of data: B.L., A.R., R.M.G., A.I.N., and P.H.G. Drafting of the manuscript: B.L. and A.R. Critical revision of the manuscript for important intellectual content: B.L., A.R., A.I.N., R.M.G., R.C.K., P.H.G., D.S., and N.S.L. Statistical analysis: A.R. Interpretation of data and approval of the final version of the manuscript: B.L., A.R., A.I.N., R.M.G., R.C.K., P.H.G., D.S., and N.S.L. Obtainment of funding: B.L. Administrative, technical, or material support: N/A. Study supervision: A.R.
B.L. was supported by the National Center for Advancing Translational Sciences, National Institutes of Health (KL2 TR000081) and A.R. by NCRR (5UL1RR024156).
Footnotes
Conflicts of interest
Dr Green is a consultant for Shire and Alba Therapeutics and is on the Scientific Advisory Board of Alvine Pharmaceuticals. Dr Genta is an employee of Miraca Life Sciences. Dr Kapel has previously served as a paid consultant to Miraca Life Sciences. For the remaining authors there are no conflicts of interest.
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