Short and Long-Term Follow-Up and Clinical Outcomes in Patients with Celiac Disease in a Large Private Practice Setting

doi:10.21203/rs.3.rs-1975890/v1

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Short and Long-Term Follow-Up and Clinical Outcomes in Patients with Celiac Disease in a Large Private Practice Setting

https://doi.org/10.21203/rs.3.rs-1975890/v1

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Journal Publication

published 11 Jan, 2023

Read the published version in BMC Gastroenterology →

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Background

Celiac disease (CD) is caused by an immune response to gluten and treatment is adherence to a gluten-free diet. Guidelines from studies in large academic settings recommend registered dietitian (RD) referrals at time of diagnosis and periodic testing for micronutrient deficiencies. There is limited data to guide follow-up parameters in a large, community-based practice. The purpose of this study was to evaluate guideline adherence in this setting.

Methods

This retrospective study assessed CD care based on follow-up rates, micronutrient testing, symptoms, and serology results in cohorts with and without RD referrals. Patients in this study are followed at Rockford Gastroenterology Associates (RGA): a large, private GI practice. Patients were included if they had a diagnosis from 1/2014 through 12/2018, based on positive serology and/or duodenal biopsy. Patient data was collected by chart review and analyzed through Microsoft Excel. Fisher’s exact and Chi-square tests were used for the statistical analysis.

Results

A cohort of 126 patients met inclusion criteria. 69.8% had a RD referral. 65.9% had at least one lab test order for any of the 6 micronutrients. Of 63 patients tested for iron, 11 were iron deficient (8 with RD referral). Of 64 patients tested for vitamin D, 21 were deficient (17 with referral). 80.2% attended at least one follow-up appointment, but 34.9% had only one follow-up visit over a mean follow up duration of 5.82 months. 79 patients had follow-up data for symptoms or serology and were separated into 4 categories (with vs without RD referral): 1) asymptomatic and negative serology (32% vs 26%), 2) symptomatic and negative serology (28% vs 16%), 3) asymptomatic and positive serology (27% vs 32%), 4) symptomatic and positive serology (13% vs 26%). Category 1 yielded a fisher exact test value of 2.62 (p = .466).

Conclusions

RD referral, micronutrient testing, and close follow-up are important parameters that affect outcomes in patients with CD. Rates for dietitian referral, some micronutrient testing and follow-up visits were higher than 50%, though results from this study were not statistically significant. Further standardization of follow-up testing and monitoring for CD will help minimize discrepancies between community-based and large, academic GI practices.

Celiac disease

micronutrient

follow-up

dietitian

private practice

guidelines

CD is a chronic immune-mediated gastrointestinal illness that affects ~ 1% of patients in the United States.¹ CD is triggered by consumption of foods containing gluten (a protein in wheat, rye, and barley). The host immune response creates antibodies against tissue transglutaminase (tTG) causing an inflammatory reaction which leads to villous atrophy in the small intestine.² Patients may present with a variety of symptoms including, but not limited to, abdominal pain, diarrhea, steatorrhea, fatigue, weight loss and bloating.³

Diagnostic evaluation for CD patients includes serology testing for IgA anti-tTG antibodies, IgG anti-tTG antibodies with serum IgA levels (if a patient is suspected to be IgA deficient) and duodenal biopsy with histological analysis. To confirm a diagnosis of CD, patients must be on a gluten-containing diet prior to serology testing. Further evaluation of CD may include repeat endoscopic evaluation for tissue analysis, repeat serology for antibody detection, and bone mineral density (BMD) testing.⁴

Current treatment for CD is strict adherence to a GFD, which requires effective patient education, individual motivation, and frequent follow-up visits. Despite patients recognizing its importance, adherence to a strict GFD poses a great challenge for many people with CD.⁵ Patients with poor adherence to a GFD have reported lower scores on quality-of-life assessments⁶ and may also have an increased risk of mortality.⁷ Thus, in order to improve the quality of life and survival of CD patients it is necessary to review both initial and repeat diagnostic tests, patient outcomes, follow-up visits, and adherence to treatment recommendations. Guidelines suggest that patients should be referred to a dietician at the time of diagnosis and should be regularly check for nutritional deficiencies including iron, vitamin D, copper, zinc, folate, and vitamin B12.^4,8,9

Published studies analyzing CD progression are based in large academic settings.^6,10,11,12 There is little data on practice parameters and clinical outcomes for CD in a private practice, community-based setting.¹³ The aim of this retrospective study was to determine guideline adherence in terms of RD referral and regular follow-up by gastroenterologists in a large private practice who were taking care of CD patients.

Study Setting and Patients

Patients diagnosed with CD and followed at Rockford Gastroenterology Associates between January 1st, 2014, and December 31st, 2018, were analyzed. A total of 126 patients met criteria and were included in the analysis. Inclusion criteria: 1) patients must be diagnosed with CD based on positive serologic testing and/or duodenal biopsy and 2) patients must be established at Rockford Gastroenterology Associates. Exclusion criteria: 1) patients who did not have a definitive diagnosis of CD based on diagnostic parameters including serology and/or biopsy evaluation. (Fig. 1)

Data Extraction and Database Creation

Patient data was collected from medical records at RGA. Demographic information, including age, gender, ethnicity, family history of CD and past medical history of autoimmune disease were documented. Initial and follow-up symptoms were recorded if documented. Data was gathered regarding referral rates to a RD at the time of diagnosis, anti-tTG antibody serology results, small intestinal biopsy/histology results, and frequency of follow-up visits. Additionally we analyzed micronutrient ordering and testing rates at diagnosis and follow up. We also looked at rates of repeat endoscopy at follow up. Finally, patients were categorized into four categories based on follow-up symptoms and serology: 1) Asymptomatic and negative tTG serology, 2) Symptomatic and negative tTG serology, 3) Asymptomatic and positive tTG serology, 4) Symptomatic and positive tTG serology.¹⁴

Statistical Analysis

Patient data was analyzed through SPSS and these variables included demographic characteristics, diagnostic findings, reported follow-up visits, and level of repeat testing (if any). Analysis was primarily descriptive and rates of follow-up and response to the GFD among these patients were compared to published literature from large academic centers. In addition, the relationship between symptomatic or histologic response to treatment and the rate of clinical and endoscopic follow was assessed. The fishers exact test and Chi-square tests were used for categorical variables. A Chi-square test was used only if null hypothesis expected values were greater than 5.

Patients

From a total of 320 patients initially identified from the EMR at RGA, a total of 126 patients were confirmed to be diagnosed between January 1, 2014, and December 31, 2018 and met inclusion criteria for this study. In this cohort, 84 (66.7%) were female, 118 (93.7%) were between the ages of 26 and 80, 117 (92.9%) were Caucasian, 23 (18.3%) reported a history of autoimmune disease (Rheumatoid arthritis, Hashimoto’s thyroiditis, Systemic lupus erythematous, etc.) and 16 (12.7%) reported a family history of CD. The baseline characteristics are detailed in Table 1.

Dietitian Referral

A total of 88 (69.8%) patients had a documented referral to a dietitian.

Follow-up Visits

101 (80.2%) patients attended at least one follow-up appointment and 57 patients (45.2%) had at least two (Fig. 2). In this cohort, 73 (52.9%) patients were also referred to a dietitian. Of the 80.2% that attended at least one follow-up appointment, 43.6% had only one with 50.5% occurring at 3 or more months after diagnosis. For the first follow-up visit, the average and median time interval after initial diagnosis were 5.82 months and 3 months, respectively. (Figure S2)

Initial and Follow-up Symptoms

Abdominal Pain

Abdominal pain was reported by 48 patients at the initial encounter. 32 of these patients did not report abdominal pain at follow-up. In the cohort of patients with at least one follow-up appointment (n = 101), 80 patients did not report abdominal pain at follow-up. 56 patients were referred to a dietitian and did not have follow-up abdominal pain. (X² = 0.996, p = 0.318)

Bloating

Bloating was reported by 32 patients at the initial encounter. 21 of these patients did not report bloating at follow-up. In the cohort of patients with at least one follow-up appointment, 91patients did not report bloating at follow-up. 64 patients were referred to a dietitian and did not have follow-up bloating. (Fisher’s exact, p = 0.276)

Flatulence

Flatulence was reported by 9 patients at the initial encounter. 6 of these patients did not report flatulence at follow-up. In the cohort of patients with at least one follow-up appointment, 98 patients did not report flatulence at follow-up. 71 patients were referred to a dietitian and did not have follow-up flatulence. (Fisher’s exact, two-sided p = 1.00)

Diarrhea

Diarrhea was reported by 62 patients at the initial encounter. 34 of these patients did not report diarrhea at follow-up. In the cohort of patients with at least one follow-up appointment, 82 patients did not report diarrhea at follow-up. 59 patients were referred to a dietitian and did not have follow-up diarrhea. (X² = 0.023, p = 0.879)

Weight Loss

Weight loss was reported by 32 patients at the initial encounter. 19 of these patients did not report weight loss at follow-up. In the cohort of patients with at least one follow-up appointment, 94 patients did not report weight loss at follow-up. 69 patients were referred to a dietitian and did not have follow-up weight loss. (Fisher’s exact, two-sided p = 0.393)

Nausea

Nausea was reported by 26 patients at the initial encounter. 14 of these patients did not report nausea at follow-up. In the cohort of patients with at least one follow-up appointment, 97 patients did not report nausea at follow-up. 70 patients were referred to a dietitian and did not have follow-up nausea. (Fisher’s exact, p = .276)

Fatigue

Fatigue was reported by 32 patients at the initial encounter. 26 of these patients did not report fatigue at follow-up. In the cohort of patients with at least one follow-up appointment, 103 patients did not report fatigue at follow-up. 75 patients were referred to a dietitian and did not have follow-up fatigue. (Fisher’s exact, two-sided p = 0.279)

*The data regarding initial and follow-up symptoms does not include data for those without a follow-up visit to record symptoms. (See Table S1, Table S2 and Figure S1)

Initial and Follow-up Serology and Biopsy

A total of 125 patients had an initial serology order/test with 105 (83.3%) at RGA and 20 (15.9%) at another facility prior to consult. 17 patients had negative initial serology results and 2 patients had normal initial biopsy results. 88 (69.8%) patients did have a repeat lab order for a follow-up serology test. 79 patients had a follow-up serology result in the EMR, 60 (75.0%) of which were referred to a dietitian. 24 of these patients had abnormal serology and 36 had normal serology. (X² = 1.371, p = 0.242) 126 patients had an initial biopsy with histological analysis. (Table 2) 22 patients had a repeat endoscopy, and 21 patients had a repeat biopsy result. 10 patients with both initial and follow-up endoscopy with biopsy showed improvement either from complete or partial changes to normal duodenal mucosa. Other data for follow-up serology and biopsy results are shown in Table S3 and Table S4.

Micronutrients

Iron

Initial iron studies (iron/ferritin) were ordered for 62 patients and follow-up iron studies were ordered for 76 patients. 77 patients were initially tested for iron studies and 63 patients were tested at follow-up. Of those tested initially, 42 (33.3%) had results within normal limits. 20 of the patients with normal initial results were not deficient at follow-up and 20 of the patients that were initially deficient were not deficient at follow-up. 6 patients remained deficient. Of the 62 tested at follow-up, 51 had results within normal limits and 11 patients were deficient. 37 patients had a dietitian referral and were tested but not deficient. 42 total patients were not tested at follow-up. (X² = 0.017, p = 0.992)

Vitamin D

Initial Vitamin D studies were ordered for 62 patients and follow-up iron studies were ordered for 76 patients. 73 patients were initially tested for Vitamin D and 64 patients were tested at follow-up. Of those tested initially, 30 (23.8%) had results within normal limits. 14 of the patients with normal initial results were not deficient at follow-up and 15 of the patients that were initially deficient were not deficient at follow-up. 12 patients remained deficient. Of those tested at follow-up, 43 had results within normal limits and 21 were deficient. 62 patients were not tested at follow-up. (X² = 4.36, p = 0.113)

Folate and Vitamin B12

Initial folate studies were ordered for 48 patients and follow-up folate studies were ordered for 44 patients. 53 patients were initially tested for folate and 40 patients were tested at follow-up. Of those tested initially, 49 (38.9%) had results within normal limits. 15 of the patients with normal initial results were not deficient at follow-up. Of those tested at follow-up, 37 had results within normal limits and 3 were deficient. 86 patients were not tested at follow-up. (Fisher’s Exact, two-sided p = 0.448)

Initial Vitamin B12 studies were ordered for 54 patients and follow-up Vitamin B12 studies were ordered for 46 patients. 64 patients were initially tested for Vitamin B12, and 44 patients were tested at follow-up. Of those tested initially, 59 (46.8%) had results within normal limits. 22 of the patients with normal initial results were not deficient at follow-up. Of those tested at follow-up, 41 had results within normal limits and 3 were deficient. 82 patients were not tested at follow-up. (Fisher’s Exact, two-sided p = 0.461)

Copper and Zinc

Initial copper studies were ordered for 18 patients and follow-up copper studies were ordered for 14 patients. 15 patients were initially tested for copper and 14 patients were tested at follow-up. Both patients that were initially deficient were not tested at follow-up. Of those tested at follow-up, 14 had results within normal limits. 112 patients were not tested at follow-up. (Fisher’s Exact, two-sided p = 0.225)

Initial zinc studies were ordered for 36 patients and follow-up zinc studies were ordered for 30 patients. 33 patients were initially tested for zinc and 26 patients were tested at follow-up. Of those tested initially, 27 (21.4%) had results within normal limits. 2 of the patients with normal initial results were not deficient at follow-up and 3 of the patients that were initially deficient were not deficient at follow-up. Of those tested at follow-up, 22 patients had a dietitian referral and were tested but not deficient, whereas 3 patients without a referral were tested but not deficient. 100 patients were not tested at follow-up. (Fisher’s Exact, two-sided p = 1.000)

*Data for micronutrients is shown in Table 3, Table S5 and Table S6.

Follow-up Categories

In the cohort of 79 patients that had follow-up data for both symptoms and serology results, 60 also had a referral to a dietitian. 24 patients were asymptomatic with normal serology, 19 of which had a dietitian referral. 13 patients were symptomatic with abnormal serology, 5 of which did not have a referral (Fig. 3). (Fisher’s Exact = 2.62, two-sided p = 0.466)

The principal finding of this study was that referral rates to a dietitian based on a documented referral or order in the EMR was much higher than expected (69.8%). Providers at RGA ordered iron (53.2%) and Vitamin D (60.3%) studies at rates greater than the hypothesized values. Testing rates for iron studies (50.0%) were equal to the hypothesized value and Vitamin D studies (50.8%) were greater than the hypothesized value. However, order and testing rates were lower than the hypothesized values for copper, zinc, folate, and Vitamin B12. There was also an increase in iron and Vitamin D studies order rates between initial and follow-up evaluation. Overall rates for micronutrient deficiencies were low without an identifiable trend when comparing patients with or without a dietitian referral. However, rates of all micronutrient deficiencies declined over time in patients that had both an initial and follow-up value. These trends were most prominently seen for iron and Vitamin D studies most likely because of the higher rates of testing in comparison to the other micronutrients (similar trend to results seen in a previously conducted study by Deora et al.).¹⁵

Follow-up visit rates at 3–6 months and beyond (50.5%) were greater than hypothesized. Time intervals between the initial diagnosis and subsequent follow-up visits (if any) were highly variable and may reflect other gastrointestinal comorbidities or other unique circumstances for some patients. Currently, guidelines set forth by AGA and the NIH recommend periodic follow-up visits at regular time intervals with both a practicing physician and a nutritionist/dietitian.^6,11 Patients that had a documented dietitian referral had higher rates of asymptomatic disease in comparison to those without a documented referral. Additionally, patients with a referral had higher rates of negative serology (anti-tTG antibody) at follow-up in comparison to those without a referral.

Although the originally hypothesized number of patients was 320 based on initial polling from the EMR, only 126 met criteria for the study. Many patient charts lacked significant data for inclusion in the analysis, which excluded them from the study analysis. Therefore, the small number of subjects made it difficult to draw statistically significant conclusions. Also, with an uneven percentage of subjects referred to a dietitian compared to those not referred (69.8% vs 30.2%), the analyses using separated cohorts furthered this discrepancy.

Other limitations of this study include the following: lack of controlling for other gastrointestinal comorbidities, lack of ability to track patient actually had a follow-up visit with a dietitian, lack of ability to track patient follow-up with their primary care provider, lack of standardization of national guideline adherence in current practice at RGA, difficulty in standardizing data input procedure regarding patient visits (i.e. symptom data in HPI vs ROS vs assessment area, results data in progress notes vs results section in EMR vs outside uploaded document), lack of ability to track follow-up for patients diagnosed near the end of the set timeframe (closer to December 2018). Without standardization in these protocols, data gathering becomes increasingly difficult as it was with this study and minimizes chance of producing statistically significant data. Additionally, there are many other micronutrients that are recommended for monitoring that were not analyzed in this study.

One discrepancy found during the analysis was the difference between micronutrient order rates and actual testing rates. There are several variables that affect these outcomes, many of which may be perceived as difficult to control for. However, a possible future improvement in CD practice and patient outcomes may include new technology, like artificial intelligence or a mobile application that tracks the variables analyzed in this study. These advances can help providers monitor patients in the outpatient setting more closely by mitigating the communication setbacks in the current healthcare system. For example, providers can monitor dietitian follow-up appointments and GFD adherence with this technology in a more efficient manner. This incorporation of technology was shown to be very effective for monitoring of other chronic diseases and improving patient quality of life.^16,17,18

Currently, most studies analyzing follow-up outcomes for patients with CD have been conducted at larger, academic centers.^6,10,11,12 Patients in this study, at a large, community-based gastroenterology practice, showed an improvement in symptomology, biopsy/histology findings, serology results and micronutrient deficiencies between the initial visit and most recent follow-up visits. Although this data was not statistically significant, these identified trends may be due to the strong dietitian referral rates and high rates of medical follow-up. These improvements may highlight underlying themes of strong clinical practice including patient motivation and encouragement as well as access to a support network. While difficult to control for, these are all factors that ultimately help patients with CD adhere appropriately to a GFD.

In summary, although Rockford Gastroenterology Associates has shown an overall strong adherence to the national guidelines set forth for diagnosis and management of patients with CD, there is much room for improvement. When analyzing each of the previous parameters individually, it was clear that clinical practice is highly variable. The gastroenterologists at RGA completed training at several different, large academic centers at different points in time. Compounding this with differences in clinical judgement, it is simple to understand that this variability is partially inevitable. However, moving forward it is important to improve standardization in management guidelines for clinical practice at RGA. Future prospective studies, like that conducted by Zanini et al.¹³, controlling for the limitations previously mentioned in community-based gastroenterology practices can help align the future of CD management in these settings with that of larger, academic centers.^6,10,11,12 The hope is to improve the overall quality of life for patients with CD by enhancing the comprehensive approach to medical management these patients require.

Registered dietitian referral, micronutrient testing, and close follow-up are important parameters that affect outcomes in patients with CD. The rates for dietitian referral, some micronutrient testing and follow-up visits were higher than 50%. Although a greater percentage of patients with a dietitian referral were asymptomatic and/or had negative serology, this was not statistically significant. Additionally, although not statistically significant, trends in this study highlight a large variability in follow-up time intervals and micronutrient lab testing. Further standardization of follow-up testing and monitoring for CD will help minimize discrepancies noted between community-based GI practices and large, academic centers.

Celiac disease (CD), Registered dietitian (RD), Gastroenterology (GI), Rockford Gastroenterology Associates, ltd. (RGA), gluten-free diet (GFD), history of present illness (HPI), review of systems (ROS), electronic medical record (EMR), tissue transglutaminase (tTG), bone mineral density (BMD)

Ethics approval and consent to participate

This project was a retrospective chart review that did not involve any experiments on humans and/or human tissue samples. All methods carried out for this project were in accordance with relevant guidelines and regulations. All experimental protocols for this project were reviewed and verified by the Institutional Review Board at the University of Illinois College of Medicine. The need to obtain informed consent was waived by the Institutional Review Board at the University of Illinois College of Medicine.

Consent for publication

Not applicable.

Availability of data and materials

The database used for this study is available upon request from the authors in the format of a Microsoft Excel file. Authors from this study will be able to electronically deliver the database. Please contact the corresponding author, Dr. Chandrashekhar Thukral, MD PhD at [email protected].

Competing interests

There were no financial and non-financial competing interests to declare.

Funding

Funding for this study was provided by the University of Illinois College of Medicine at Rockford, Department of Research, and the research division at RGA.

Authors’ contributions

AK performed the chart review, created the database, created tables/graphs and wrote the manuscript. CT was the primary advisor for the project, edited the manuscript and coordinated any funding required from RGA. DL provided scientific method guidance for the statistical analysis and data for the initial literature review. KG aided with the statistical analysis.

Acknowledgements

Not applicable.

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Tables 1 to 3 are available in the Supplementary Files section.

No competing interests reported.

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Journal Publication

published 11 Jan, 2023

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Editorial decision: Major revision
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You are reading this latest preprint version

Short and Long-Term Follow-Up and Clinical Outcomes in Patients with Celiac Disease in a Large Private Practice Setting

Status:

Journal Publication

Version 1

Abstract

Background

Methods

Results

Conclusions

Figures

Background

Methods

Study Setting and Patients

Data Extraction and Database Creation

Statistical Analysis

Results

Patients

Dietitian Referral

Follow-up Visits

Initial and Follow-up Symptoms

Abdominal Pain

Bloating

Flatulence

Diarrhea

Weight Loss

Nausea

Fatigue

Initial and Follow-up Serology and Biopsy

Micronutrients

Iron

Vitamin D

Folate and Vitamin B12

Copper and Zinc

Follow-up Categories

Discussion

Conclusions

Abbreviations

Declarations

References

tables

Additional Declarations

Supplementary Files

Status:

Journal Publication

Version 1