Abstract
Background
Fragmented care for inflammatory bowel disease (IBD) is known to correlate negatively with outcomes, but it is unclear which aspects of care fragmentation are relevant and potentially modifiable. Furthermore, there is little data on the relationship between travel distance and the benefits of integrated care models. Hypothesizing care coordination in the preoperative period may have a significant impact on surgical outcomes, we explored associations between integrated care, travel distance, and surgical outcomes.
Methods
A single-center retrospective cohort study of patients undergoing index abdominal surgery was done to compare the rate of surgical complications with and without long travel distance and nonintegrated preoperative care. Multivariable logistic regression was used to identify factors independently associated with complications.
Results
One hundred and fifty-seven patients were included. Complications were more common among patients with travel distance >75 miles (47.6% vs 27.4%, P = .012). Integrated preoperative care was not significant on bivariate (P = .381) or multivariable analysis but had a stronger association among patients with travel distance <75 miles (20.9% integrated vs 36.7%, P = .138). After adjustment, new ileostomy, open surgical approach, and distance >75 miles were independently associated with complications.
Conclusions
Patients with longer travel distances to the hospital were twice as likely to have a surgical complication after adjusting for other risk factors. Without significant accommodations for remote patients, potential benefits of an integrated model for IBD care may be limited to patients who live close to the medical center. Future efforts addressing continuity of care should consider tactics to mitigate the impact of travel distance on outcomes.
Keywords: inflammatory bowel disease, fragmentation, travel distance, surgery, disparities
Graphical Abstract
Graphical Abstract.
Introduction
Inflammatory bowel diseases (IBD) consist of Crohn’s disease (CD) and ulcerative colitis (UC), chronic and morbid conditions affecting an estimated 3 million people in the United States and often leading to high healthcare costs, particularly through inpatient, medication, and procedural expenses.1 A multidisciplinary approach involving gastroenterologists and colorectal surgeons is a mainstay of management. Given the unique behavioral, preventative, and therapeutic requirements for patients with IBD, their care is taking place increasingly within patient-centered specialty medical homes that include not only expert IBD physicians, but also behavioral health specialists, nurse coordinators, dietitians, social workers, and advanced practice providers.2 As the complexity of care puts patients at risk for segmentation and fragmentation, there is increasing support for integrated IBD care and population-based care delivery models.3,4
Readmission to a non-index hospital after surgery has a well-established association with increased mortality in a wide variety of conditions.5–9 For nonsurgical IBD admissions, over one-in-four readmissions occurs in a non-index hospital and this fragmentation is associated with increased length of stay and mortality.3 Thus, there is strong evidence to promote continuity of care after major episodes of care involving hospitalization or surgery. However, it is less clear what impact integrated care (or its inverse) prior to surgery has on outcomes. Given the complex and multidisciplinary inputs involved in the timing of surgery for IBD and in preoperative optimization (eg, nutritional support, correction of anemia), effective care coordination before surgery may play an even larger role compared with coordination in follow-up.
Fragmented care for IBD may also contribute to disparities, particularly in the outcomes of surgery. IBD patients with markers of low socioeconomic status are more likely to experience surgical complications.10 Similarly, they are more likely to have 90-day readmission to a non-index hospital.3 Increasing regional consolidation of specialty care also poses unique challenges in access to care for rural patients, for whom fragmentation may be a major driver in outcome disparities.11–13 Accordingly, travel distance is correlated with readmission to a non-index hospital after surgery.9 Better health outcomes are generally observed with shorter travel distances, although results of these analyses are frequently confounded by the beneficial effect of receiving care at high-volume centers.14,15 There is a paucity of data on the effect of travel distance for IBD surgery outcomes, especially in the United States.10
The goal of this study was to explore the role of integrated care for IBD before surgery and its association with surgical outcomes. Secondarily, we sought to identify patient factors associated with nonintegrated care as a potentially modifiable mechanism for disparities based on socioeconomic and geographic factors.
Methods
Patients and Data Collection
This was a single-center retrospective cohort study. Our institutional clinical data warehouse was queried to identify patients with an International Classification of Diseases (ICD) diagnosis code for IBD who had a Current Procedural Terminology (CPT) code indicative of intestinal surgery (colectomy, proctectomy, ostomy) between January 2015 and December 2020. For patients with multiple operations during the study period, only the first encounter for surgery was included in the analysis; for example, for staged ileal-pouch anal anastomosis, the initial episode for colectomy was considered for inclusion. Patients with incident IBD defined as disease duration less than 1 year were excluded.
Patient characteristics and operative details were obtained from manual review of the electronic health record. The indication for surgery in the operative report was used to determine the IBD diagnosis of CD, UC, or indeterminate colitis. The extent and timing of gastroenterology management prior to surgery was established by reviewing the health record for previous clinic notes. Straight-line travel distance between the hospital and patient residence was calculated using the geographic center of patient zip codes. Likewise, 9-digit zip codes were used to determine the national percentile rank (1–100) for area deprivation index (ADI),16,17 a multidimensional measure of socioeconomic status derived from neighborhood-level census data that is highly correlated with a wide variety of health outcomes.18 Institutional Review Board approval for a waiver of informed consent was obtained.
All surgeries were performed by one of 2 fellowship-trained colorectal surgeons. To the extent feasible, perioperative management followed an institutional enhanced recovery protocol for colorectal surgery. Specific protocol elements evolved over the research period but were generally in line with established guidelines.19 For example, components maintained over the study period included preoperative carbohydrate loading, restrictive intra- and postoperative IV fluid administration, avoidance of routine drains and nasogastric tubes, early feeding, early ambulation, and minimization of narcotics.
Outcomes and Definitions
The primary outcome was a composite of postoperative complications. These included (1) requirement for postoperative blood transfusion; (2) surgical site infection (SSI) including anastomotic leak, abscess or deep SSI, and superficial wound infection; (3) enterocolitis due to C. difficile within 30 days; (4) ostomy complications including high output ileostomy and requirement for operative revision; (5) emergency department (ED) visit within 30 days of index surgery; (6) unplanned return to OR within 30 days; (7) unplanned readmission within 90 days; (8) mortality within 90 days. Other less common but standardly recorded postoperative complications such as urinary tract infection, pneumonia, stroke, and myocardial infarction were also included. Postoperative clinic and telephone notes were reviewed for documentation of complications that were managed at external facilities.
Covariates: Integrated Gastroenterology Care and Travel Distance
The main exposures were the absence of specialist gastroenterology (GI) care at the institution where surgery was performed and travel distance over 75 miles from the hospital. Integrated GI care was defined by the presence of at least 2 outpatient medical GI physician or advanced practice provider encounters (ie, not infusions alone) in the year prior to surgery at the same institution where surgery was performed. Outpatient GI medicine and surgery clinic visits occurred at the main hospital campus or at an off-campus clinic in the immediate suburban area (all less than 10 miles away from the main hospital). In addition to an IBD nurse coordinator, a dedicated IBD pharmacist and behavioral health social worker were added to the clinic staff during the study period. Telemedicine encounters were rarely utilized prior to the COVID-19 pandemic and while included as potential preoperative visits, did not contribute significantly to the presence or absence of preoperative care integration.
Other covariates are listed in Table 1. These included age, gender, race, ADI, elective vs nonelective surgery, IBD disease type, procedure, and surgical approach. Biologic medication use was defined as active on therapy within 1 month of surgery; chronic steroid use was defined as any dose for at least 3 consecutive months immediately prior to surgery; high-dose steroid was at least 20 mg prednisone or equivalent within 2 weeks of surgery. Malnutrition included a composite of body mass index (BMI) <18.5 kg m−2, preoperative (within 1 month) albumin <3.0 g L−1, or >10% body weight loss within 6 months. Anemia was defined as preoperative hemoglobin <12 g dL−1 for women and <13 g dL−1 for men. Given the relatively broad range of colorectal procedures in the study (eg, ileocolic resection with primary anastomosis vs subtotal colectomy with end ileostomy), we did not evaluate anastomotic technique as a risk factor.
Table 1.
Comparison of (1) patients with and without preoperative continuity of gastroenterology care and (2) patients with residential distance greater than versus less than 75 miles from the hospital.
| Total cohort N = 157 |
Nonintegrated GI care N = 82 |
Integrated GI care N = 75 |
P | Over 75 miles N = 84 |
Under 75 miles N = 73 |
P | |
|---|---|---|---|---|---|---|---|
| Age (years); median [IQR] | 48 [31.5–58.5] | 50.5 [34–60] | 44 [29–56] | .118 | 47.5 [32–59] | 49 [30.5–58] | .912 |
| IBD duration (years); median [IQR] | 11 [4.5–20] | 12.5 [5–25] | 10 [4–19] | .140 | 11 [4–20] | 12 [5–21.5] | .325 |
| Distance (miles); median [IQR] | 77.5 [19.4–103] | 81 [46–106] | 66 [18–103] | .052 | 102 [82–117] | 19 [8–51] | <.001 |
| Gender | .709 | .438 | |||||
| Male | 61 (38.9) | 33 (40.2) | 28 (37.3) | 35 (41.7) | 26 (35.6) | ||
| Female | 96 (61.1) | 49 (59.8) | 47 (62.7) | 49 (58.3) | 47 (64.4) | ||
| Race | .443 | .961 | |||||
| White | 122 (77.7) | 67 (81.7) | 55 (73.3) | 66 (78.6) | 56 (76.7) | ||
| Black | 33 (21.0) | 14 (17.1) | 19 (25.3) | 17 (20.2) | 16 (21.9) | ||
| Other | 2 (1.3) | 1 (1.2) | 1 (1.3) | 1 (0.6) | 1 (0.6) | ||
| Area deprivation index | .521 | <.001 | |||||
| 1st quartile (least deprived) | 16 (10.2) | 11 (13.4) | 5 (6.7) | 1 (1.2) | 15 (20.5) | ||
| 2nd quartile | 59 (37.6) | 31 (37.8) | 28 (37.3) | 31 (36.9) | 28 (38.4) | ||
| 3rd quartile | 43 (27.4) | 21 (25.6) | 22 (29.3) | 26 (31.0) | 17 (23.3) | ||
| 4th quartile (most deprived) | 38 (24.2) | 18 (22.0) | 20 (26.7) | 26 (31.0) | 12 (16.4) | ||
| Missing | 1 (0.6) | 1 (0.6) | 0 (0) | 0 (0) | 1 (1.4) | ||
| Case status | .015 | .482 | |||||
| Elective | 123 (78.3) | 58 (70.7) | 65 (86.7) | 64 (76.2) | 59 (80.8) | ||
| Nonelective | 34 (21.7) | 24 (29.3) | 10 (13.3) | 20 (23.8) | 14 (19.2) | ||
| Disease type | .843 | .616 | |||||
| Crohn’s disease | 117 (74.5) | 60 (73.2) | 57 (76.0) | 60 (71.4) | 57 (78.1) | ||
| Ulcerative colitis | 37 (23.6) | 20 (24.4) | 17 (22.7) | 22 (26.2) | 15 (20.5) | ||
| Indeterminate colitis | 3 (1.9) | 2 (2.4) | 1 (1.3) | 2 (2.4) | 1 (1.4) | ||
| Previous major surgery | .087 | .647 | |||||
| Yes | 48 (30.6) | 30 (36.6) | 18 (24.0) | 27 (32.1) | 21 (28.8) | ||
| No | 109 (69.4) | 52 (63.4) | 57 (76.0) | 57 (67.9) | 52 (71.2) | ||
| Indication | .971 | .357 | |||||
| Obstruction | 68 (43.3) | 35 (42.7) | 33 (44.0) | 33 (39.3) | 35 (47.9) | ||
| Fistula/abscess | 32 (20.4) | 16 (19.5) | 16 (21.3) | 16 (19.0) | 16 (21.9) | ||
| Neoplasm/malignancy | 14 (8.9) | 8 (9.8) | 6 (8.0) | 7 (8.3) | 7 (9.6) | ||
| Medically refractory disease | 43 (27.4) | 23 (28.0) | 20 (26.7) | 28 (33.3) | 15 (20.5) | ||
| Approach | .551 | .882 | |||||
| Laparoscopic | 130 (82.8) | 66 (80.5) | 64 (85.3) | 69 (53.1) | 61 (46.9) | ||
| Open | 17 (10.8) | 11 (13.4) | 6 (8.0) | 10 (11.9) | 7 (9.6) | ||
| Converted | 10 (6.4) | 5 (6.1) | 5 (6.7) | 5 (6.0) | 5 (6.8) | ||
| Procedure | .192 | .167 | |||||
| Partial resection | 117 (74.5) | 59 (72.0) | 58 (77.3) | 59 (70.2) | 58 (79.5) | ||
| Total colectomy | 33 (21.0) | 17 (20.7) | 16 (21.3) | 19 (22.6) | 14 (19.2) | ||
| Ostomy | 7 (4.5) | 6 (7.3) | 1 (1.3) | 6 (7.1) | 1 (1.4) | ||
| New ileostomy | .322 | .071 | |||||
| Yes | 50 (31.8) | 29 (35.4) | 21 (28.0) | 32 (38.1) | 18 (24.7) | ||
| No | 107 (68.2) | 53 (64.6) | 54 (72.0) | 52 (61.9) | 55 (75.3) | ||
| New colostomy | .544 | ||||||
| Yes | 13 (8.3) | 9 (11.0) | 4 (5.3) | 8 (9.5) | 5 (6.8) | ||
| No | 144 (91.7) | 73 (89.0) | 71 (94.7) | 76 (90.5) | 68 (93.2) | ||
| ASA disease classification | .059 | .212 | |||||
| II | 83 (52.9) | 36 (43.9) | 47 (62.7) | 39 (46.4) | 44 (60.3) | ||
| III | 72 (45.9) | 45 (54.9) | 27 (36.0) | 44 (52.4) | 28 (38.4) | ||
| IV | 2 (1.3) | 1 (1.2) | 1 (1.3) | 1 (1.2) | 1 (1.4) | ||
| Integrated GI care | NA | .009 | |||||
| Yes | 75 (47.8) | 32 (38.1) | 43 (58.9) | ||||
| No | 82 (52.2) | 52 (61.9) | 30 (41.1) | ||||
| Distance >75 miles | .009 | NA | |||||
| Yes | 84 (53.5) | 52 (63.4) | 32 (42.7) | ||||
| No | 73 (46.5) | 30 (36.6) | 43 (57.3) | ||||
| Biologic medication | .002 | .474 | |||||
| Yes | 114 (72.6) | 51 (62.2) | 63 (84.0) | 59 (70.2) | 55 (75.3) | ||
| No | 43 (27.4) | 31 (37.8) | 12 (16.0) | 25 (29.8) | 18 (24.7) | ||
| Chronic steroids | .229 | .853 | |||||
| Yes | 18 (11.5) | 7 (8.5) | 11 (14.7) | 10 (11.9) | 8 (11.0) | ||
| No | 139 (88.5) | 75 (91.5) | 64 (85.3) | 74 (88.1) | 65 (89.0) | ||
| High-dose steroid | .384 | .275 | |||||
| Yes | 34 (21.7) | 20 (24.4) | 14 (18.7) | 21 (25.0) | 13 (17.8) | ||
| No | 123 (78.3) | 62 (75.6) | 61 (81.3) | 63 (75.0) | 60 (82.2) | ||
| Preoperative opioid use | .126 | .930 | |||||
| Yes | 55 (35.3) | 24 (29.6) | 31 (41.3) | 29 (34.9) | 26 (35.6) | ||
| No | 101 (64.7) | 57 (70.4) | 44 (58.7) | 54 (65.1) | 47 (64.4) | ||
| Preoperative anemia | .123 | .060 | |||||
| Yes | 75 (47.8) | 44 (53.7) | 31 (41.3) | 46 (54.8) | 29 (39.7) | ||
| No | 82 (52.2) | 38 (46.3) | 44 (58.7) | 38 (45.2) | 44 (60.3) | ||
| Preoperative malnutrition | .293 | .605 | |||||
| Yes | 59 (37.6) | 34 (41.5) | 25 (33.3) | 30 (35.7) | 29 (39.7) | ||
| No | 98 (62.4) | 48 (58.5) | 50 (66.7) | 54 (64.3) | 44 (60.3) | ||
| Smoking | .109 | .327 | |||||
| Yes | 17 (10.8) | 12 (14.6) | 5 (6.7) | 11 (13.1) | 6 (8.2) | ||
| No | 140 (89.2) | 70 (85.4) | 70 (93.3) | 73 (86.9) | 67 (91.8) | ||
| Obesity (BMI >30 kg m−2) | .909 | .656 | |||||
| Yes | 32 (20.4) | 17 (20.7) | 15 (20.0) | 16 (19.0) | 16 (21.9) | ||
| No | 125 (79.6) | 65 (79.3) | 60 (80.0) | 68 (81.0) | 57 (21.9) | ||
| Number of comorbidities | .723 | .091 | |||||
| 0 | 105 (66.9) | 53 (64.6) | 52 (69.3) | 50 (59.5) | 55 (75.3) | ||
| 1 | 32 (20.4) | 17 (20.7) | 15 (20.0) | 22 (26.2) | 10 (13.7) | ||
| 2+ | 20 (12.7) | 12 (14.6) | 8 (10.7) | 12 (14.3) | 8 (11.0) | ||
Abbreviations: ASA, American Society of Anesthesiologists; BMI, body mass index; IBD, inflammatory bowel disease. Values are shown as column totals N (%) unless otherwise specified.
Statistical Analysis
Bivariate analyses were performed using chi-square or Fisher’s exact tests for categorical variables and Mann–Whitney U-tests for continuous variables, as appropriate. After assessing for collinearity between candidate variables, covariates plausibly associated with increased risk of postoperative complications and statistical significance P < .05 were entered into a multivariable logistic regression model. Final model inputs were identified using backward stepwise elimination. A planned subgroup analysis was performed to examine the interaction between care integration and travel distance on surgical complications. A multiplicative interaction term was added to the final logistic regression model to determine if the association between integrated care and complications varied by travel distance >75 miles. All analyses were conducted using IBM SPSS Statistics version 28.0 (IBM Corp.).
Sensitivity Analyses
We also completed a series of sensitivity analyses to test whether the results would change with more restricted criteria for the composite outcome or definition of care integration. First, we examined the multivariable model with the dependent variable as the composite of SSI and readmission instead of any complication. Second, continuity of GI care was defined as having at least 1 preoperative outpatient visit rather than 2 in the year preceding surgery. Finally, we examined whether the proportion of patients with a complication was significantly different when the cutoff for travel distance was changed from 75 miles to 50 and 100 miles.
Results
Cohort Characteristics
Two hundred and twenty-one patients with the appropriate ICD and CPT codes were screened for eligibility. Forty-seven were excluded for a missing or unclear diagnosis of IBD as the general indication for surgery. Seventeen patients with incident IBD (<1 year duration) were excluded, leaving 157 patients for the analysis. Patients with CD (74.5%) were more common than those with UC (23.6%). Accordingly, 21% of patients underwent total colectomy; 74.5% had a partial bowel resection. The remaining 4.5% had an ostomy for diversion without bowel resection. The type of IBD was highly correlated with procedure and indication: most patients with UC underwent total colectomy for medically refractory disease. Fifty patients (32%) had a new ileostomy, including 29 of 37 patients with UC (78.4%) and 19 of 117 patients with CD (16.2%).
Characteristics by Integrated Care and Travel Distance
The distribution of patients by the number of outpatient GI encounters in the year prior to surgery is shown in Figure 1. Eighty-two patients (52.2%) designated as having “Nonintegrated GI Care” had less than 2 GI encounters prior to surgery. Of those, 53 had no prior outpatient medical GI encounter within the hospital system. Eighty-four of 157 patients (53.5%) had residence over 75 miles from the surgical center. Patients with nonintegrated GI care were more likely to live >75 miles from the hospital (P = .009). Characteristics of the cohort and comparisons by the presence of integrated GI care and travel distance >75 miles are shown in Table 1. Patients with nonintegrated GI care had higher surgical acuity as represented by a greater proportion of patients undergoing nonelective surgery (29.3% vs 13.3%, P = .015 and marginally higher American Society of Anesthesiology (ASA) disease classification (P = .059). They were also less likely to be on therapy with a biologic medication (62.2% vs 84.0%, P = .009). Those living further from the hospital were more likely to live in areas with higher levels of socioeconomic deprivation (P < .001). Remote patients had nonsignificant increases in comorbid disease burden (P = .091), preoperative anemia (P = .06), and new ileostomy (38.1% vs 24.7%, P = .071).
Figure 1.
Preoperative gastroenterology care integration. This figure shows the distribution of patients (N) by the number of outpatient gastroenterology counters in the year prior to surgery. The vertical line represents the cutoff used for integrated care. A sensitivity analysis was performed for patients with no prior GI visits (0).
Surgical Complications
Outcomes of surgery are shown in Table 2. Overall, 60 patients (38.2%) had a complication. 27.4% had either SSI and/or readmission. There were no statistically significant differences according to integrated preoperative GI care, although 30-day ED visits were marginally higher in the nonintegrated group (26.8% vs 14.7%, P = .062). Total composite complications were significantly higher among patients living over 75 miles from the hospital, (47.6% vs 27.4%, P = .009), as were the composite of SSI and 90-day readmission (P = .012), as well as SSI alone (P = .014).
Table 2.
Outcomes of surgery comparing (1) patients with and without integrated gastroenterology care and (2) patients with residential distance greater than versus less than 75 miles from the hospital.
| Total cohort N = 157 |
Nonintegrated GI care N = 82 |
Integrated GI care N = 75 |
P | Over 75 miles N = 84 |
Under 75 miles N = 73 |
P | |
|---|---|---|---|---|---|---|---|
| Postoperative LOS | 5 [4–8] | 4.5 [4–8.25] | 5 [4–7] | .699 | 5 [4–10] | 4 [4–7] | .151 |
| Complication | |||||||
| Bleedinga | 20 (12.7) | 13 (15.9) | 7 (9.3) | .221 | 15 (17.9) | 5 (6.8) | .039 |
| SSIb | 25 (12.7) | 15 (18.3) | 10 (13.3) | .396 | 19 (22.6) | 6 (8.2) | .014 |
| C. difficile colitis | 3 (1.9) | 0 | 3 (4.0) | .069 | 2 (2.4) | 1 (1.4) | .653 |
| Ostomy complication | 10 (6.4) | 5 (6.1) | 5 (6.7) | .884 | 4 (4.8) | 6 (8.2) | .376 |
| VTE | 7 (4.5) | 4 (4.9) | 3 (4.0) | .790 | 5 (6.0) | 2 (2.7) | .331 |
| Otherc | 7 (4.5) | 4 (4.9) | 3 (4.0) | .790 | 4 (4.8) | 3 (4.1) | .843 |
| 30-Day ED visit | 33 (21.0) | 22 (26.8) | 11 (14.7) | .062 | 21 (25.0) | 12 (16.4) | .189 |
| 90-Day readmission | 33 (21.0) | 21 (25.6) | 12 (16.0) | .140 | 21 (25.0) | 12 (16.4) | .189 |
| 30-Day return to OR | 4 (2.5) | 2 (2.4) | 2 (2.7) | .928 | 2 (2.4) | 2 (2.7) | .887 |
| 90-Day mortality | 2 (1.3) | 1 (1.2) | 1 (1.3) | .949 | 2 (2.4) | 0 | .185 |
| Composite: SSI/readmission | 43 (27.4) | 26 (31.7) | 17 (22.7) | .205 | 30 (35.7) | 13 (17.8) | .012 |
| Composite: any complication | 60 (38.2) | 34 (41.5) | 26 (34.7) | .381 | 40 (47.6) | 20 (27.4) | .009 |
Abbreviations: ED, emergency department; LOS, length of stay (days); OR, operating room; SSI, surgical site infection; UTI, urinary tract infection; VTE, venous thromboembolism. All values expressed as column totals N (%) except LOS as median [IQR].
aDefined as receipt of at least 1 postoperative blood transfusion.
bIncluded deep surgical site infection (abscess, infected fluid collection; 20 total), superficial wound infection (3), and anastomotic leak (1).
cIncluded urinary tract infection (3), pneumonia (2), stroke (1), and acute kidney injury (1). One patient with “Other” complication (UTI) was included in the composite outcome without any other inclusion criteria (eg, readmission).
A complete comparison of patients with and without a complication is shown in Table 3. After excluding variables with a high degree of collinearity (indication and procedure with UC; high-dose steroids with chronic steroids), the characteristics significantly associated with a complication were entered into a multivariable logistic regression model. Unadjusted odds ratios (ORs) and 95% CIs for all candidate variables are shown in Table 4 with the adjusted ORs for final model predictors after stepwise elimination. The c-statistic for model fit was 0.748. Factors independently associated with composite complication risk were open surgical approach (OR 3.15, 95% CI: 1.23–8.11), new ileostomy (3.85, 1.79–8.30), and travel distance >75 miles (2.17, 1.01–4.63).
Table 3.
Comparison of patients with and without a postoperative complication.
| Total cohort N = 157 |
Any complication N = 60 |
No complication N = 97 |
P | |
|---|---|---|---|---|
| Age (years); median [IQR] | 48 [31.5–58.5] | 47.5 [33–58.5] | 48 [30.5–58.5] | .935 |
| IBD duration (years); median [IQR] | 11 [4.5–20] | 9 [3–20] | 12 [5.5–21] | .065 |
| Integrated GI care | .381 | |||
| Yes | 75 (47.8) | 26 (43.3) | 49 (50.5) | |
| No | 82 (52.2) | 34 (56.7) | 48 (49.5) | |
| Distance >75 miles | .009 | |||
| Yes | 84 (53.5) | 40 (66.7) | 44 (45.4) | |
| No | 73 (46.5) | 20 (33.3) | 53 (54.6) | |
| Sex | .570 | |||
| Male | 61 (38.9) | 25 (41.7) | 36 (37.1) | |
| Female | 96 (61.1) | 35 (58.3) | 61 (62.9) | |
| Race | .918 | |||
| White | 122 (77.7) | 47 (78.3) | 75 (77.3) | |
| Black | 33 (21.0) | 12 (20.0) | 21 (21.6) | |
| Other | 2 (1.3) | 1 (1.7) | 1 (1.0) | |
| Area deprivation index | .731 | |||
| 1st quartile (least deprived) | 16 (10.2) | 5 (8.3) | 11 (11.3) | |
| 2nd quartile | 59 (37.6) | 22 (36.7) | 37 (38.1) | |
| 3rd quartile | 43 (27.4) | 17 (28.3) | 26 (26.8) | |
| 4th quartile (most deprived) | 38 (24.2) | 15 (25.0) | 23 (23.7) | |
| Missing | 1 (0.6) | 1 (100) | 0 | |
| Case status | .017 | |||
| Elective | 123 (78.3) | 41 (68.3) | 82 (84.5) | |
| Nonelective | 34 (21.7) | 19 (31.7) | 15 (15.5) | |
| Disease type | .010 | |||
| Crohn’s disease | 117 (74.5) | 38 (63.3) | 79 (81.4) | |
| Ulcerative colitis | 37 (23.6) | 19 (31.7) | 18 (18.6) | |
| Indeterminate colitis | 3 (1.9) | 3 (5.0) | 0 | |
| Previous major surgery | .902 | |||
| Yes | 48 (30.6) | 18 (30.0) | 30 (30.9) | |
| No | 109 (69.4) | 42 (70.0) | 67 (69.1) | |
| Indication | .021 | |||
| Obstruction | 68 (43.3) | 18 (30.0) | 50 (51.5) | |
| Fistula/abscess | 32 (20.4) | 13 (21.7) | 19 (19.6) | |
| Neoplasm/malignancy | 14 (8.9) | 5 (8.3) | 9 (9.3) | |
| Medically refractory disease | 43 (27.4) | 24 (40.0) | 19 (19.6) | |
| Approach | .035 | |||
| Laparoscopic | 130 (82.8) | 44 (73.3) | 86 (88.7) | |
| Open | 17 (10.8) | 11 (18.3) | 6 (6.2) | |
| Converted | 10 (6.4) | 5 (8.3) | 5 (5.2) | |
| Procedure | .031 | |||
| Partial resection | 117 (74.5) | 38 (63.3) | 79 (81.4) | |
| Total colectomy | 33 (21.0) | 19 (31.7) | 14 (14.4) | |
| Ostomy | 7 (4.5) | 3 (5.0) | 4 (4.1) | |
| New ileostomy | <.001 | |||
| Yes | 50 (31.8) | 31 (51.7) | 19 (19.6) | |
| No | 107 (68.2) | 29 (48.3) | 78 (80.4) | |
| New colostomy | .226 | |||
| Yes | 13 (8.3) | 7 (11.7) | 6 (6.2) | |
| No | 144 (91.7) | 53 (88.3) | 91 (93.8) | |
| ASA disease classification | .820 | |||
| II | 83 (52.9) | 30 (50.0) | 53 (54.6) | |
| III | 72 (45.9) | 29 (48.3) | 43 (44.3) | |
| IV | 2 (1.3) | 1 (1.7) | 1 (1.0) | |
| Biologic medication | .598 | |||
| Yes | 114 (72.6) | 45 (75.0) | 69 (71.1) | |
| No | 43 (27.4) | 15 (25.0) | 28 (28.9) | |
| Chronic steroids | .008 | |||
| Yes | 18 (11.5) | 12 (20.0) | 6 (6.2) | |
| No | 139 (88.5) | 48 (80.0) | 91 (93.8) | |
| High-dose steroid | .027 | |||
| Yes | 34 (21.7) | 19 (31.7) | 15 (15.5) | |
| No | 123 (78.3) | 41 (68.3) | 82 (84.5) | |
| Preoperative opioid use | .185 | |||
| Yes | 55 (35.3) | 25 (41.7) | 30 (31.3) | |
| No | 101 (64.7) | 35 (58.3) | 66 (68.8) | |
| Preoperative anemia | .006 | |||
| Yes | 75 (47.8) | 37 (61.7) | 38 (39.2) | |
| No | 82 (52.2) | 23 (38.3) | 59 (60.8) | |
| Preoperative malnutrition | .011 | |||
| Yes | 59 (37.6) | 30 (50.0) | 29 (29.9) | |
| No | 98 (62.4) | 30 (50.0) | 68 (70.1) | |
| Smoking | .793 | |||
| Yes | 17 (10.8) | 6 (10.0) | 11 (11.3) | |
| No | 140 (89.2) | 54 (90.0) | 86 (88.7) | |
| Obesity (BMI >30 kg m−2) | .753 | |||
| Yes | 32 (20.4) | 13 (21.7) | 19 (19.6) | |
| No | 125 (79.6) | 47 (78.3) | 78 (80.4) | |
| Number of comorbidities | .983 | |||
| 0 | 105 (66.9) | 40 (66.7) | 65 (61.9) | |
| 1 | 32 (20.4) | 12 (20.0) | 20 (20.4) | |
| 2+ | 20 (12.7) | 8 (13.3) | 12 (12.4) |
Abbreviations: ASA, American Society of Anesthesiologists; BMI, body mass index; IBD, inflammatory bowel disease. Values are shown as column totals N (%) unless otherwise specified.
Table 4.
Unadjusted and adjusted odds ratios for composite complication.
| Unadjusted OR (95% CI) |
Adjusted OR (95% CI) |
+ Interaction OR (95% CI) |
|
|---|---|---|---|
| Integrated GI care | 0.75 (0.39–1.43) | 0.74 (0.53–2.44) | 2.11 (0.78–5.70) |
| Distance >75 miles | 2.41 (1.23–4.70) | 2.17 (1.01–4.63) | 1.02 (0.35–2.95) |
| Open approach (vs laparoscopic) | 2.84 (1.22–6.65) | 3.15 (1.23–8.11) | 3.47 (1.32–9.11) |
| Ulcerative colitis (vs not UC) | 2.19 (1.03–4.65) | ||
| Nonelective surgery | 2.41 (1.23–4.70) | 2.27 (0.95–5.41) | 2.15 (0.90–5.15) |
| New ileostomy | 4.39 (2.15–8.95) | 3.85 (1.79–8.3) | 4.28 (1.94–9.46) |
| Chronic steroids | 3.79 (1.34–10.73) | ||
| Anemia | 2.50 (1.29–4.84) | ||
| Malnutrition | 2.35 (1.20–4.57) | ||
| Distance <75 miles × integrated care a | 0.33 (0.14–0.74) | 0.22 (0.047–1.04) |
Abbreviation: UC, ulcerative colitis. Covariates in the model after backward stepwise elimination are presented with adjusted odds ratios. In the final iteration, an interaction term for travel distance >75 miles and integrated care was added to the previous model. Odds ratios for statistically significant covariates in the multivariable models are shown in bold.
aAll covariates shown were entered into the initial multivariable logistic regression model except for the interaction term.
Interaction Between Travel Distance and Care Integration
Among patients with travel distance under 75 miles, 36.7% of patients without integrated GI care had a complication compared with 20.9% of patients with integrated care (P = .138). For patients over 75 miles, no discernible effect was observed: 44.2% complication rate for nonintegrated care vs 53.1% for integrated care, P = .428. Examined in the inverse, for the subgroup of patients with integrated GI care, complications were significantly more common for those with travel distance >75 miles (53.1% vs 20.9%, P = .004). For patients without integrated care, there was no difference in complication rate according to travel distance (44.2% vs 36.7%, P = .503). When added to the full logistic regression model (Table 4), the interaction term between travel distance and care integration was not statistically significant (P = .056).
Sensitivity Analyses
The logistic regression analysis was repeated with composite SSI and readmission as the dependent variable. New ileostomy (2.60, 1.20–5.63), open surgical approach (2.97, 1.19–7.41), and travel distance over 75 miles (2.23, 1.02–4.87) remained associated with the composite outcome in the final model. Defining integrated preoperative GI care as having no prior outpatient encounter for IBD medical management did not reveal a significant association with composite complication risk (41.4% nonintegrated vs 37.5% integrated, P = .698). Finally, we examined travel distance for a potential dose–response effect. As a continuous variable, distance from the hospital was significantly associated with composite complications (P = .031). When examined as a categorical variable with cutoffs of 50, 75, and 100 miles, the proportion with a complication in the more remote group was 43.3% (P = .068), 47.6% (P = .009), and 46.5% (P = .189), respectively.
Discussion
Fragmentation of care is a major concern among patients and health system stakeholders due to the attendant inefficiencies, increased costs, and worse health outcomes. Postoperative care fragmentation in the form of readmission to a non-index hospital after major surgery is a clear source of morbidity. Given the chronicity of IBD, the coordination of care occurring prior to surgery may have an even greater impact on outcomes. In IBD, the decision to operate is uniquely multidisciplinary, and optimizing a patient for surgery requires close collaboration between surgeons, gastroenterologists, and other team members. In this retrospective cohort, we hypothesized patients who received their medical management for IBD at the same institution where surgery is performed would have fewer complications than patients with less integrated care. We found within-institution GI care before surgery did not have a significant correlation with outcomes. However, we did identify an association between travel distance and surgical complications. After controlling for acuity, surgical approach, and the requirement for an ileostomy, patients traveling over 75 miles for surgery were twice as likely to have a complication.
There is strong evidence for significant disparities in IBD surgery outcomes based on race and socioeconomic status, but existing data for differences by geographic factors are very limited.10 An analysis of colectomy for UC in the National Inpatient Sample found mortality was higher at rural hospitals, but less than 4% of operations occurred at rural locations.20 Unfortunately, most nationally representative databases lack the granularity necessary to explore travel distance as a contributor to outcomes. Our data highlight the need for further attention in this area among researchers and clinicians. As care for IBD becomes increasingly specialized and concentrated in high-volume centers, it is important to consider the burdens that regionalization puts on patients in remote locations. In many parts of the country, including ours, the majority of specialty care patients live far from their nearest specialty care medical home.21 Lack of consistent access may hinder them from realizing the benefits of a potentially higher standard of care.
There are number of factors that could explain the lack of a significant difference based on care integration, and the most obvious is sample size. We did observe a difference in the direction of our hypothesis, but the effect of integrated care was not large enough to be statistically significant. As an exploratory study with a set number of patients available to study, we did not perform an a priori power calculation. With a group size of 75 patients and the complication proportions we observed (22.7% integrated and 31.7% nonintegrated), the study power was 23%. Three hundred and eighty-three patients would be required in each group to achieve 80% power. It is notable that ED visits, a metric closely related to access issues, did approach a significant association (26.8% nonintegrated vs 14.7% integrated, P = .062). Second, the definition of integrated care as operationalized by within-institution outpatient GI visits before surgery may not accurately reflect the impact of care coordination prior to surgery. Specifically, patients with high number of GI visits prior to surgery may have had a more severe disease phenotype, a possible source of uncontrolled confounding. Finally, the impact of care integration on complication rate may interact significantly with travel distance. Potential benefits of integrated care for IBD may not accrue to patients who live remotely.
Considering other definitions for care continuity, readmission to a non-index hospital is a commonly used indicator of fragmentation but was rare in this cohort and fails to address the concept of preoperative care integration. Other investigators with a more global view of fragmentation have used network analysis methods to examine the association between interprovider connectedness and the risk of IBD flares or need for surgery, observing that higher connectedness is generally correlated with better outcomes.22 While this approach has generated valuable insight, it can be difficult to interpret clinically: it remains unclear which interprovider connections are most relevant for patient outcomes and whether the timing of these encounters matters. The same holds true for analyses of large administrative datasets using other global measures of fragmentation, such as the Bice–Boxerman continuity of care index.23 These efforts have revealed a critical need to address fragmented care for IBD, but it is unclear which aspects of care delivery are relevant and potentially modifiable.24 We believe the perioperative period, often an inflection point in overall disease management, represents 1 area where concerted efforts at care coordination may have a major impact on patient outcomes. Further study is needed to align populations who may benefit from such efforts with the appropriate model for care delivery.
Our findings underscore the importance of tailoring care to the needs of the population served. A fully integrated specialty care medical home may be ideal for patients who live locally but aggravate access issues for remote patients. Over half of our cohort traveled over 75 miles for surgery. Independent of other risk factors, remote patients had worse outcomes, and nonintegrated care was correlated with travel distance >75 miles. However, it remains unclear whether a lack of integrated care contributes to worse surgical outcomes for remote patients. Travel distance >75 miles may function as a proxy for other risk factors, both observed and unobserved, and these may or may not be modifiable through more effective care integration. Remote patients had greater comorbid disease burden (P = .091), more preoperative anemia (P = .060), and increased likelihood of an ileostomy (P = .071). Preoperative anemia, the most modifiable among these, could be attributed to differences in IBD severity, management, or to other comorbid disease, thus effective recognition and treatment may not automatically follow from optimal perioperative IBD care. Although ADI did not correlate with surgical outcomes, it is notable that its distribution varied significantly by travel distance (P < .001). Other unmeasured confounders related to social and structural barriers in rural health are likely active, but it is unclear how this disparity in surgical outcomes can be addressed. Future studies regarding the continuity of care for IBD should incorporate geographic data (eg, travel distance) whenever available.
In addition to the sample size limitations and exploratory, retrospective nature of this study, the generalizability may be narrow. As alluded to above, travel distance >75 miles may be acting as an instrumental variable for some other confounder that is unique to the geography and demographics of SC. Furthermore, the utilization of individual components of integrated care (eg, nutritional support, behavioral therapy, medication assistance, and adherence) are not measured routinely in our practice. Thus, we were not able to include these as process measures for effective care coordination in our study. However, despite these limitations, our results are suggestive of a broad and under-appreciated challenge in the management of rural populations.25 Further consolidation of services (eg, behavioral therapy, IBD-primary care) under the umbrella of an IBD specialty medical home may not benefit these patients without significant accommodations for remote patients.26,27 Integrated care models for IBD involving enhanced telemedicine capabilities28,29 or rural-based integrated care27 warrant further attention.
Conclusions
Patients with longer travel distances to the hospital were twice as likely to have a surgical complication after adjusting for other risk factors. Integrated preoperative IBD care was not associated with a decreased risk of surgical complications but may have a differential effect based on distance from the hospital. Future efforts addressing continuity of care should include consideration for travel distance as a potential confounder. Ultimately, a larger study with a multicenter approach is needed to determine the effect of integrated preoperative care on surgical outcomes for IBD.
Contributor Information
Alexander Booth, Division of Colon and Rectal Surgery, Medical University of South Carolina, Charleston, South Carolina, USA; Health Equity and Rural Outreach Innovation Center, Ralph H. Johnson Department of Veterans Affairs Medical Center, Charleston, South Carolina, USA.
Henry Colorado, Division of Colon and Rectal Surgery, Medical University of South Carolina, Charleston, South Carolina, USA.
Gayenell Magwood, College of Nursing, Medical University of South Carolina, Charleston, South Carolina, USA.
Erin Forster, Division of Gastroenterology, Hepatology and Nutrition, Medical University of South Carolina, Charleston, South Carolina, USA.
Robert N Axon, Health Equity and Rural Outreach Innovation Center, Ralph H. Johnson Department of Veterans Affairs Medical Center, Charleston, South Carolina, USA.
Thomas Curran, Division of Colon and Rectal Surgery, Medical University of South Carolina, Charleston, South Carolina, USA.
Funding
This work was supported by a VA Health Services Research and Development Charleston Health Equity and Rural Outreach Innovation Center (HEROIC) SWIFT Pilot Grant [CIN 13-410] to A.B., as well as the VA Quality Scholars fellowship, through the VA Office of Academic Affiliations Advanced Fellowships Program. The content is solely the responsibility of the authors and does not necessarily represent the official views of the VA Quality Scholars or the Department of Veterans Affairs.
Authors’ Contributions
A.B. and T.C. conceived the study question. A.B., T.C., and E.F. designed the study. A.B. and H.C. acquired the data. A.B. analyzed the data. All authors contributed to data interpretation. A.B. drafted the manuscript. All authors reviewed the manuscript for intellectual content and approved the final version.
Conflicts of Interest
E.F. holds the position of Associate Editor for Crohn’s & Colitis 360 and has been recused from reviewing or making decisions for the manuscript. Otherwise, the authors have no relevant disclosures.
Data Availability
Data not publicly available.
References
- 1. Dahlhamer JM, Zammitti EP, Ward BW, Wheaton AG, Croft JB.. Prevalence of inflammatory bowel disease among adults aged ≥18 years—United States, 2015. MMWR Morb Mortal Wkly Rep. 2016;65(42):1166–1169. [DOI] [PubMed] [Google Scholar]
- 2. Regueiro M, Click B, Holder D, Shrank W, McAnallen S, Szigethy E.. Constructing an inflammatory bowel disease patient-centered medical home. Clin Gastroenterol Hepatol. 2017;15(8):1148–1153.e4. [DOI] [PubMed] [Google Scholar]
- 3. Cohen-Mekelburg S, Rosenblatt R, Gold S, et al. Fragmented care is prevalent among inflammatory bowel disease readmissions and is associated with worse outcomes. Am J Gastroenterol. 2019;114(2):276–290. [DOI] [PubMed] [Google Scholar]
- 4. Nguyen NH, Luo J, Ohno-Machado L, Sandborn WJ, Singh S.. Burden and outcomes of fragmentation of care in hospitalized patients with inflammatory bowel diseases: a nationally representative cohort. Inflamm Bowel Dis. 2021;27(7):1026–1034. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Juo YY, Sanaiha Y, Khrucharoen U, Chang BH, Dutson E, Benharash P.. Care fragmentation is associated with increased short-term mortality during postoperative readmissions: a systematic review and meta-analysis. Surgery. 2019;165(3):501–509. [DOI] [PubMed] [Google Scholar]
- 6. McCrum ML, Cannon AR, Allen CM, Presson AP, Huang LC, Brooke BS.. Contributors to increased mortality associated with care fragmentation after emergency general surgery. JAMA Surg. 2020;155(9):841–848. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Zafar SN, Shah AA, Channa H, Raoof M, Wilson L, Wasif N.. Comparison of rates and outcomes of readmission to index vs nonindex hospitals after major cancer surgery. JAMA Surg. 2018;153(8):719–727. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Beal EW, Bagante F, Paredes A, et al. Index versus non-index readmission after hepato-pancreato-biliary surgery: where do patients go to be readmitted? J Gastrointest Surg. 2019;23(4):702–711. [DOI] [PubMed] [Google Scholar]
- 9. Tsai TC, Orav EJ, Jha AK.. Care fragmentation in the postdischarge period surgical readmissions, distance of travel, and postoperative mortality. JAMA Surg. 2015;150(1):59–64. [DOI] [PubMed] [Google Scholar]
- 10. Booth A, Ford W, Brennan E, Magwood G, Forster E, Curran T.. Towards equitable surgical management of inflammatory bowel disease: a systematic review of disparities in surgery for inflammatory bowel disease. Inflamm Bowel Dis. 2022;28(9):1405–1419. [DOI] [PubMed] [Google Scholar]
- 11. Borren NZ, Conway G, Tan W, et al. Distance to specialist care and disease outcomes in inflammatory bowel disease. Inflamm Bowel Dis. 2017;23(7):1234–1239. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Jackson KL, Glasgow RE, Hill BR, et al. Does travel distance influence length of stay in elective colorectal surgery? Dis Colon Rectum. 2013;56(3):367–373. [DOI] [PubMed] [Google Scholar]
- 13. Benchimol EI, Kuenzig ME, Bernstein CN, et al. Canadian Gastro-Intestinal Epidemiology Consortium. Rural and urban disparities in the care of Canadian patients with inflammatory bowel disease: a population-based study. Clin Epidemiol. 2018;10:1613–1626. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Kelly C, Hulme C, Farragher T, Clarke G.. Are differences in travel time or distance to healthcare for adults in global north countries associated with an impact on health outcomes? A systematic review. BMJ Open. 2016;6(11):e013059. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Diaz A, Cloyd JM, Manilchuk A, et al. Travel patterns among patients undergoing hepatic resection in California: does driving further for care improve outcomes? J Gastrointest Surg. 2021;25(6):1471–1478. [DOI] [PubMed] [Google Scholar]
- 16. University of Wisconsin School of Medicine and Public Health. 2015 Area Deprivation Index v20. Vol 2020. 2015. https://www.neighborhoodatlas.medicine.wisc.edu/. Accessed March 15, 2022. [Google Scholar]
- 17. Kind AJH, Buckingham W.. Making neighborhood disadvantage metrics accessible: the neighborhood atlas. New Engl J Med. 2018;378(26):2456–2458. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Michaels AD, Meneveau MO, Hawkins RB, Charles EJ, Mehaffey JH.. Socioeconomic risk-adjustment with the area deprivation index predicts surgical morbidity and cost. Surgery. 2021;170(5):1495–1500. [DOI] [PubMed] [Google Scholar]
- 19. Carmichael JC, Keller DS, Baldini G, et al. Clinical practice guidelines for enhanced recovery after colon and rectal surgery from the American Society of Colon and Rectal Surgeons and Society of American Gastrointestinal and Endoscopic Surgeons. Dis Colon Rectum. 2017;60(8):761–784. [DOI] [PubMed] [Google Scholar]
- 20. Olaiya B, Renelus BD, Filon M, Saha S.. Trends in morbidity and mortality following colectomy among patients with ulcerative colitis in the biologic era (2002–2013): a study using the National Inpatient Sample. Dig Dis Sci. 2021;66(6):2032–2041. [DOI] [PubMed] [Google Scholar]
- 21. Diaz A, Schoenbrunner A, Pawlik TM.. Trends in the geospatial distribution of inpatient adult surgical services across the United States. Ann Surg. 2021;273(1):121–127. [DOI] [PubMed] [Google Scholar]
- 22. Cohen-Mekelburg S, Yu X, Costa D, et al. Variation in provider connectedness associates with outcomes of inflammatory bowel diseases in an analysis of data from a national health system. Clin Gastroenterol Hepatol. 2021;19(11):2302–2311.e1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. Cohen-Mekelburg S, Saini SD, Krein SL, et al. Association of continuity of care with outcomes in US veterans with inflammatory bowel disease. JAMA Netw Open. 2020;3(9):e2015899. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24. Fudman DI, Hou JK.. Fragmentation, care models, and improving outcomes in inflammatory bowel disease. JAMA Netw Open. 2020;3(9):e2016122. [DOI] [PubMed] [Google Scholar]
- 25. Xu F, Carlson SA, Liu Y, Greenlund KJ.. Urban–rural differences in health care utilization for inflammatory bowel disease in the USA, 2017. Dig Dis Sci. 2021;67(8):3601–3611. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26. Brunt H, Chapman JC.. The inflammatory bowel disease-focused primary care provider: an addition to the IBD specialty medical home. Am J Gastroenterol. 2022;117(2):209–212. [DOI] [PubMed] [Google Scholar]
- 27. Watt P. Recommendations for the provision of psychological support in a rural inflammatory bowel disease clinic. Inflamm Bowel Dis. 2019;25(11):e149–e150. [DOI] [PubMed] [Google Scholar]
- 28. de Jong MJ, Boonen A, van der Meulen-de Jong AE, et al. Cost-effectiveness of telemedicine-directed specialized vs standard care for patients with inflammatory bowel diseases in a randomized trial. Clin Gastroenterol Hepatol. 2020;18(8):1744–1752. [DOI] [PubMed] [Google Scholar]
- 29. Zand A, Nguyen A, Stokes Z, et al. Patient experiences and outcomes of a telehealth clinical care pathway for postoperative inflammatory bowel disease patients. Telemed e-Health. 2020;26(7):889–897. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Data not publicly available.