Kuenzig ME, Bitton A, Carroll MW, Otley AR, Singh H, Kaplan GG, Stukel TA, Mack DR, Jacobson K, Griffiths AM, El Matary W, Targownik LE, Nguyen GC, Jones JL, Murthy SK, Bernstein CN, Lix LM, Pena Sanchez JN, Dummer TJB, Spruin S, Fung SG, Nugent Z, Coward S, Cui Y, Coulombe J, Filiter C, Benchimol EI. Health services utilization and specialist care in pediatric inflammatory bowel disease: A multiprovince population-based cohort study. Inflammatory Bowel Diseases 2024; 30(12):2356-2369.

 

Background: Patterns of health services utilization among children with IBD are important to understand as the number of children with IBD continues to increase. We compared health services utilization and surgery among children diagnosed younger than 10 years of age (Paris classification: A1a) and between 10 and 16 years of age (A1b).

Methods: Newly diagnosed cases of IBD diagnosed less than 16 years of age were identified using validated algorithms from deterministically linked health administrative data in 5 Canadian provinces (Alberta, Manitoba, Nova Scotia, Ontario, Quebec) to conduct a retrospective cohort study. We compared the frequency of IBD-specific outpatient visits, emergency department visits, and hospitalizations across age groups (A1a vs A1b [reference]) using negative binomial regression. The risk of surgery was compared across age groups using Cox proportional hazards models. Models were adjusted for sex, rural/urban residence location, and mean neighborhood income quintile. Province-specific estimates were pooled using random-effects meta-analysis.

Results: Among the 1165 (65.7% Crohn's disease) children with IBD included in our study, there were no age differences in the frequency of hospitalizations (rate ratio [RR], 0.88; 95% confidence interval [CI], 0.74-1.06) or outpatient visits (RR, 0.95; 95% CI, 0.78-1.16). A1a children (less than 10 years at diagnosis) had 30% fewer emergency department visits (RR, 0.70; 95% CI, 0.50-0.97) and were 50% less likely to require a Crohn's-related surgery (hazard ratio, 0.49; 95% CI, 0.26-0.92). The risk of colectomy was similar among children with ulcerative colitis in both age groups (hazard ratio, 0.71; 95% CI, 0.49-1.01).

Conclusions: Patterns of health services utilization are generally similar when comparing children diagnosed across age groups, although children diagnosed before age 10 with Crohn’s disease were less likel to have a Crohn’s disease related surgery.

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Coward S, Benchimol EI, Bernstein CN, Avina-Zubieta A, Bittonn A, Carroll MW, Cui Y, Hoentgen F, Hracs L, Jacobson K, Jones JL, King K, Kuenzig ME, Lu N, El Matary W, Murthy S, Otley A, El Matary W, Nugent Z, Otley AR, Panaccione R, Peña-Sánchez JN, Singh H, Targownik LE, White D, Windsor JW, Kaplan GG on behalf of the Canadian Gastro-Intestinal Epidemiology Consortium (CanGIEC). Forecasting the incidence and prevalence of inflammatory bowel disease: A Canadian nationwide analysis. American Journal of Gastroenterology 2024; Aug 1;119(8):1563-1570.

 

Introduction: Canada has a high burden of IBD. Historical trends of IBD incidence and prevalence were analyzed to forecast the Canadian burden over the next decade.

Methods: Population-based surveillance cohorts in 8 provinces derived from health administrative data assessed the national incidence (newly diagnosed cases) (2007-2014) and prevalence (all known cases, newly and previously diagnosed) (2002-2014) of IBD. Autoregressive integrated moving average models were used to forecast incidence and prevalence, stratified by age, with 95% prediction intervals (PI), to 2035. The average annual percentage change (AAPC) with 95% confidence interval (CI) was calculated for the forecasted incidence and prevalence.

Results: The national incidence of IBD is estimated to be 29.9 per 100,000 (95% PI 28.3-31.5) in 2023. With a stable AAPC of 0.36% (95% CI -0.05 to 0.72), the incidence of IBD is forecasted to be 31.2 per 100,000 (95% PI 28.1-34.3) in 2035. The incidence in pediatric patients (younger than 18 years) is increasing (AAPC 1.27%; 95% CI 0.82-1.67), but it is stable in adults (AAPC 0.26%; 95% CI -0.42 to 0.82). The prevalence of IBD in Canada was 843 per 100,000 (95% PI 716-735) in 2023 and is expected to steadily climb (AAPC 2.43%; 95% CI 2.32-2.54) to 1,098 per 100,000 (95% PI 1,068-1,127) by 2035. The highest prevalence was in seniors with IBD (1,174 per 100,000 in 2023; AAPC 2.78%; 95% CI 2.75-2.81).

Conclusion: Over the next decade, the Canadian health care systems will contend with the juxtaposition of rising incidence of pediatric IBD and a rising prevalence of overall IBD driven by the aging population. Well over 1 in 100 Canadians will have a diagnosis of IBD.

 

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Buie MJ, Coward S, Shaheen AA, Holroyd-Leduc J, Hracs L, Ma C, Panaccione R, Benchimol EI, Bernstein CN, Bitton A, Otley AR, Jones JL, Murthy SK, Ellen Kuenzig M, Peña-Sánchez JN, Targownik LE, Singh H, Avina-Zubieta A, Kaplan GG. Hospitalization rates for inflammatory bowel disease are decreasing over time: A population-based cohort study. Inflammatory Bowel Diseases. 2023; Oct 3;29(10):1536-1545.

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Recent advances in the management of IBD striving for new treatment targets may have decreased rates of hospitalization for flares. We compared all-cause, IBD-related, and non-IBD-related hospitalizations while accounting for the rising prevalence of IBD. Population-based, administrative health care databases identified all individuals living with IBD in Alberta between fiscal year 2002 and 2018. Hospitalization rates (all-cause, IBD-related, and non-IBD-related) were calculated using the prevalent Alberta IBD population. Hospitalizations were stratified by disease type, age, sex, and metropolitan status. Data were age and sex standardized to the 2019 Canadian population. Log-linear models calculated Average Annual Percentage Change (AAPC) in hospitalization rates with associated 95% confidence intervals (CIs). Results: From 2002-2003 to 2018-2019, all-cause hospitalization rates decreased from 36.57 to 16.72 per 100 IBD patients (AAPC, -4.18%; 95% CI, -4.69 to -3.66). IBD-related hospitalization rate decreased from 26.44 to 9.24 per 100 IBD patients (AAPC, -5.54%; 95% CI, -6.19 to -4.88). Non-IBD-related hospitalization rate decreased from 10.13 to 7.48 per 100 IBD patients (AAPC, -1.82%; 95% CI, -2.14 to -1.49). Those over 80 years old had the greatest all-cause and non-IBD-related hospitalization rates. Temporal trends showing decreasing hospitalization rates were observed across age, sex, IBD type, and metropolitan status. We concluded that hospitalization rates are decreasing for all-cause, IBD-related, and non-IBD-related hospitalizations. Over the past 20 years, the care of IBD has transitioned from hospital-based care to ambulatory-centric IBD management.

 

 

El-Matary W, Witt J, Bernstein CN, Jacobson K, Mack D, Otley A, Walters TD, Huynh HQ, deBruyn J, Griffiths AM, Benchimol EI. Indirect and Out-Of-Pocket Disease-Associated Costs in Pediatric Inflammatory Bowel Disease: A Cross-Sectional Analysis. Journal of Pediatric Gastroenterology and Nutrition. 2022; 75: 466-472.

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Data on out of pocket (OOP) and indirect costs associated with paediatric IBD are limited. We aimed to estimate indirect and OOP costs associated with pediatric IBD in Canada. In a nation-wide cross-sectional analysis, caregivers of patients diagnosed with IBD (younger than 17y) were invited to complete a questionnaire on lost work hours and OOP costs related to IBD in the 4 weeks prior to the survey. Random participants were re-invited to answer the same questionnaire every 6-9 months for 2 years. Lost productivity was calculated using the Human Capital method and costs were reported in 2018 inflation-adjusted Canadian dollars. Predictors of high cost users (top 25%) were examined using negative binomial regression. Results: Overall, 243 of 262 (92.7%) patients completed the first survey with a total completion of 458 surveys. The median annual indirect costs per patient, using combined data from all surveys, were $5,951 (IQR $1,812- $12,278), with $5,776 (IQR $1,465-$11,733) for Crohn disease (CD) and $6,084 (IQR $2,470-$13,371) for ulcerative colitis (UC) (p = 0.77). The annual median per patient OOP costs, using all survey data, were $2,925 (IQR $978- $8,125) with $3,021 (IQR $978- $8,125) for CD and $2,600 (IQR $975- $8,125) for UC (p = 0.55). Older age at diagnosis (p=0.04) and parents in part-time employment (p=0.01) were predictors of higher indirect costs, while male patients (p<0.001), parents with a lower education level (p<0.001) and lower annual income (p<0.01) were associated with higher OOP costs. Conclusions: Indirect and OOP costs are substantial. More resources are needed particularly for those with lower family income.

 

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Buie M, Quan J, Windsor JW, Coward S, Hansen TM, King JA, Kotze PG, Gearry RB, Ng SC, Mak JWY, Abreu MT, Rubin DT, Bernstein CN, Banerjee R, Yamamoto-Furusho J, Panaccione R, Seow CH, Ma C, Underwood FE, Ahuja V, Pannaccione N, Shaeen AA, Holroyd-Leduc J, Kaplan GG, On Behalf of the GIVES-21 Consortia. Global Hospitalization Trends for Crohn’s Disease and Ulcerative Colitis in the 21 st Century: A Systematic Review with Temporal Analyses. Clinical Gastroenterology and Hepatology. 2022; Jul 19:S1542-3565(22)00670-X.

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The evolving epidemiologic patterns of IBD throughout the world, in conjunction with advances in therapeutic treatments, may influence hospitalization rates of IBD. We performed a systematic review with temporal analysis of hospitalization rates for IBD across the world in the 21st century. We systematically reviewed Medline and Embase for population-based studies reporting hospitalization rates for IBD, Crohn's disease, or ulcerative colitis in the 21st century. Log-linear models were used to calculate the average annual percentage change (AAPC) with associated 95% confidence intervals (95% CIs). Random-effects meta-analysis pooled country-level AAPCs. Data were stratified by the epidemiologic stage of a region: compounding prevalence (stage 3) in North America, Western Europe, and Oceania vs acceleration of incidence (stage 2) in Asia, Eastern Europe, and Latin America vs emergence (stage 1) in developing countries. Results: Hospitalization rates for a primary diagnosis of IBD were stable in countries in stage 3 (AAPC, -0.13%; 95% CI, -0.72 to 0.97), CD (AAPC, 0.20%; 95% CI, -1.78 to 2.17), and ulcerative colitis (AAPC, 0.02%; 95% CI, -0.91 to 0.94). In contrast, hospitalization rates for a primary diagnosis were increasing in countries in stage 2 for IBD (AAPC, 4.44%; 95% CI, 2.75 to 6.14), Crohn's disease (AAPC, 8.34%; 95% CI, 4.38 to 12.29), and ulcerative colitis (AAPC, 3.90; 95% CI, 1.29 to 6.52). No population-based studies were available for developing regions in stage 1 (emergence). Conclusions: Hospitalization rates for IBD are stabilizing in countries in stage 3, whereas newly industrialized countries in stage 2 have rapidly increasing hospitalization rates, contributing to an increasing burden on global health care systems.

 

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Shafer LA, Shaffer S, Witt J, Nugent Z, Bernstein CN. IBD Disability Index (IBDDI) is associated with both direct and indirect costs of inflammatory bowel disease. Inflammatory Bowel Diseases. 2022; 28(8):1189-1197.

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We aimed to determine both direct (medical) and indirect (lost wages) costs of IBD and the association between the degree of IBD-related disability and extent of IBD-related costs. Persons age 18-65 from the population-based University of Manitoba IBD Research Registry completed a survey including the IBD Disability Index (IBDDI) and questions related to employment, missed work (absenteeism), and reduced productivity at work (presenteeism). Administrative health data including surgeries, hospitalizations, physician claims, and prescriptions were linked to the survey and assessed. To calculate annual wage loss, number of days of missed work was multiplied by the average wage in Manitoba for the given occupation per Statistics Canada. Costs were adjusted to 2016-17 Canadian dollars. Using descriptive and regression analysis, we explored the association between IBDDI and annual direct and indirect costs associated with IBD. Results: Average annual medical costs rose from $1918 among those with IBDDI 0-4 to $9,993 among those with IBDDI 80-86. Average annual cost of lost work rose from $0 among those with IBDDI 0-4 to $30,101 among those with IBDDI 80-86. Using linear regression, each additional unit of IBDDI was associated with an increase of $77 in annual medical cost (95% CI, $52-102; P <.001) and an increase of $341 in annual cost of lost wages (95% CI, $288-395; P < .001). Conclusions: Costs related to IBD are significantly associated with the degree of IBD-related disability. Among the approximate 30% of the IBD population with IBDDI scores of at least 40, the indirect costs of absenteeism and presenteeism accounts for ~75% of the total IBD-related costs.

 

 

Tandon P, Tennakoon A, Huang V, Bernstein CN,  Goetgebuer R, Targownik L. Pregnancy and live birth rates in women with inflammatory bowel disease: A Canadian population-based cohort study. Journal of Canadian Association of Gastroenterology 2022; Mar 16;5(4):184-191.

 

IBD negatively affects fertility and fecundity. We aimed to determine longitudinal trends in and factors that affect pregnancy rates in women with ulcerative colitis and Crohn’s disease. Women in the University of Manitoba IBD Epidemiology Database aged 15-45, in Manitoba, Canada were identified between 1992-2018 and matched up to 10 non-IBD controls. Pregnancy and live birth rates were compared between women with and without ulcerative colitis or Crohn’s disease stratified by time period, disease duration, and maternal age at conception. Incidence rate ratios (IRR) with 95% confidence intervals (CI) were calculated. Poisson regression was used to adjust these rates for year of pregnancy, disease duration, maternal age, severity of IBD, and prior IBD-related surgery.  Compared to controls, women with ulcerative colitis had lower rates of pregnancies (IRR 0.91, 95% CI, 0.82-0.99) and women with Crohn’s disease had lower rates of pregnancies (IRR 0.85, 95% CI, 0.79-0.93) and live births (IRR 0.83, 95% CI, 0.75-0.92). There were no differences in rates of pregnancies between cases and controls from 2010 to 2018. Factors that significantly lowered pregnancy rates included a new IBD diagnosis and maternal age at conception less than 35 for Crohn’s disease. Furthermore, prior IBD-related surgery and active disease at conception also appeared to lower pregnancy rates in women with ulcerative colitis and Crohn’s disease respectively.

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In conclusion shorter disease duration, younger age at conception, active disease, and prior IBD-surgery negatively impact pregnancy and live birth rates in women with ulcerative colitis and Crohn’s disease. 

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Bernstein CN, Singh H, Murthy SK, Nguyen GC, Benchimol EI, Bitton A, Kuenzig ME, Huang JG, Jones JL, Lee K, Targownik LE, Windsor JW, Mukhtar MS, Tandon P, Kaplan GG. Crohn's and Colitis Canada's 2021 Impact of COVID-19 and Inflammatory Bowel Disease in Canada: Seniors With IBD.  Journal of the Canadian Association of Gastroenterology 2021 Nov 5;4(Suppl 2): S34-S39.

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The risk of hospitalization and death from COVID-19 increases with age. The extreme elderly have been particularly vulnerable, with those above the age of 80 having a case-fatality rate as high as 15%. Aging of the immune system can lead to impaired inflammatory responses where eradication of an organism such as SARS-CoV2 is inadequate but is exaggerated in such a way as to enhance pneumonia and acute respiratory distress syndrome. Frailty and comorbidity are both more common in the elderly, and these can enhance the morbidity and mortality from COVID-19. Studies from Northern California and Italy suggest that elderly persons with IBD were more likely to acquire SARS-CoV-2 infection than youths with IBD. While the specific impact of age-related comorbidity is less well established among people with IBD who acquire COVID-19, data from the Surveillance Epidemiology of Coronavirus Under Research Exclusion (SECURE-IBD) database reported that having two or more chronic illnesses was independently associated with developing severe COVID-19 among people with IBD. Despite having exaggerated auto-inflammatory responses, people with IBD do not appear to have an overall increased risk of developing severe COVID-19 than the general population. However, whether seniors with IBD do worse once they acquire COVID-19 compared with seniors without IBD is not known. The advent of telehealth care has posed an information technology challenge for many seniors with and without IBD. Most persons with IBD have expressed satisfaction with virtual IBD health care (phone or video-based visits). While the elderly may have less robust immune responses to vaccinations, learning from experiences with other vaccination programs, especially influenza, have shown that vaccinating seniors decreases both morbidity and mortality and, in turn, healthcare resources.

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Benchimol EI, Carroll MW, Geist R, Griffiths AM, Huang JG, Mack DR, Bernstein CN, Bitton A, Jones JL, Kaplan GG, Kuenzig ME, Lee K, Mukhtar MS, Murthy SK, Tandon P, Targownik LE, Windsor JW, Seow CH.  Crohn's and Colitis Canada's 2021 Impact of COVID-19 and Inflammatory Bowel Disease in Canada: Children and Expectant Mothers With Inflammatory Bowel Disease.  Journal of the Canadian Association of Gastroenterology 2021 Nov 5;4(Suppl 2): S27-S33.

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Canada has among the highest rates of IBD in the world, and the number of people living with these disorders is growing rapidly. This has placed a high burden on the health care system and on the Canadian economy-a burden that is only expected to grow in the future. It is important to understand IBD and its impact on Canadian society in order to appropriately plan for health care expenditures, reduce the burden on patients and their families, and improve the quality of life for those afflicted with IBD. In Canada, there is a lack of public awareness of the impact of Crohn's disease and ulcerative colitis. Raising awareness is crucial to reducing the social stigma that is common with these diseases and to help individuals maximize their overall quality of life. A better public understanding of IBD can also help to raise and direct funds for research, which could lead to improved treatments and, ultimately, to a cure. This report from Canadian clinicians and researchers to Crohn's and Colitis Canada makes recommendations aimed at the public, policy-makers, scientific funding agencies, charitable foundations and patients regarding future directions for advocacy efforts and areas to emphasize for research spending. The report also identifies gaps in knowledge in the fields of clinical, health systems and epidemiological research.

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Coward S, Windsor JW, Kuenzig ME, Bitton A, Bernstein CN, Jones JL, Khanna R, Lee K, Murthy SK, Targownik L, Benchimol E, Huang JG, Mukhtar MS, Tandon P, Kaplan GG. Crohn's and Colitis Canada's 2021 Impact of COVID-19 and Inflammatory Bowel Disease in Canada: Epidemiology-The Trends of Disease Over Time. Journal of the Canadian Association of Gastroenterology 2021 Nov 5;4(Suppl 2): S20-S26.

 

At the beginning of the COVID-19 pandemic, there were many unknowns: transmission vectors of the virus, appropriate intervention strategies and if being immunocompromised due to IBD, for example, or medications put a person at increased risk for severe COVID-19. Imposing and relaxing of public health restrictions at different times and in different regions in Canada led to different epidemiologies of the virus in different provinces and territories. In order to understand the waxing and waning of waves of the COVID-19 pandemic, it is necessary to understand the effective reproductive number (Rt) and the countervailing forces that exert upward or downward pressure on the spread of the virus at a given point in time. As many regions in Canada deal with a third wave, the primary forces affecting the Rt of severe acute respiratory syndrome coronavirus 2 are variants of concern and the increasing vaccinations of Canadians leading to increased population-level immunity. Fortunately, for the IBD population, current research suggests that those with IBD are not at increased risk of contracting COVID-19, nor of having a more severe disease course when compared to the general population.

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Gearry RB, McCombie AM, Vatn M, Rubin DT, Steinwurz F, Loftus EV, Kruis W, Tysk C, Colombel JF, Ng SC, Van Assche G, Bernstein CN. What are the most challenging aspects of inflammatory bowel disease? An international survey of gastroenterologists comparing developed and developing countries. Inflammatory Intestinal Diseases 2021 May;6(2):78-86.

 

As IBD becomes more prevalent, the challenges that gastroenterologists face in managing these patients evolve. We aimed to describe the most important challenges facing gastroenterologists from around the world and compare these between those working in developed and developing countries. An online questionnaire was developed, and a link distributed to gastroenterologists. Data were analyzed descriptively using Friedman and Wilcoxon matched-pair signed rank tests to compare rankings for responses. Mann-Whitney U tests were used to compare rankings between responses from gastroenterologists from developed and developing countries. Lower scores reflected greater challenges. Of 872 who started, 397 gastroenterologists (45.5%) completed the survey. Respondents represented 65 countries (226 [56.9%] from developed countries). Overall, the challenge ranked most important (smallest number) was increasing IBD prevalence (13.6%). There were significant differences in mean ranking scores for many simple aspects of care for those from developing countries compared to providers from developed countries, such as access to simple IBD treatments (5.52 vs. 6.02, p = 0.01), access to anti-TNF drugs including dose escalation (3.33 vs. 3.93, p < 0.01), access to good stoma care (2.57 vs. 3.03, p < 0.001), access to therapeutic drug monitoring (1.47 vs. 1.84, p < 0.001), and access to care for people from low socioeconomic status (2.77 vs. 3.37, p < 0.001).

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Increasing IBD prevalence is seen by gastroenterologists as the greatest challenge facing them. There are significant differences between the IBD challenges facing gastroenterologists from developed and developing countries that reflect inequities in access to health care.

 

 

El-Matary W, Nugent Z, Witt J, Bernstein CN. Trends in paediatric inflammatory bowel disease-attributable direct costs: a population-based analysis. Alimentary Pharmacology and Therapeutics 2021; 53(11):1201-1208. 

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In addition to its morbidities, inflammatory bowel disease (IBD) has a major financial burden on patients and healthcare systems. However, there is a paucity of evidence on IBD-attributable costs in children. We aimed to determine the trends of IBD-attributable direct costs over time using a population-based analysis. Data were extracted from Manitoba Health administrative health database and other population registry datasets from 1995 to 2017. Children with IBD were matched by age, sex and location with children without IBD. IBD-attributable direct costs were calculated using utilization counts from the administrative data and cost estimates from different sources. Inpatient hospitalisation and outpatient procedure costs were estimated using the resource intensity weight that is attached to each record in the data. Costs were expressed in Canadian dollars. We included 733 (428 with Crohn's disease) prevalent cases who were diagnosed with IBD before the age of 18 years and were followed for 2450 person-years. A matched control group of 6763 persons who were followed for 21 558 person-years was included. The median annual costs of physician services billed per patient increased from $381 (IQR 215-1064) in 1995 to $936 (IQR 579-1932) in 2017 (P < 0.001). The annual medication costs per patient increased from a median of $270 in 1995 to $7944 in 2017 (P < 0.0001). The median annual direct cost per patient was $1810 in 2004 as compared to $14 791 (P < 0.0001) in 2017.

Over two decades, there was a significant increase in the paediatric IBD-attributable direct costs mainly driven by medication costs.

 

 

Bernstein CN, Hitchon CA, Walld R, Bolton JM, Lix LM, El-Gabalawy R, Sareen J, Singer A, Katz A, Marriott J, Fisk JD, Patten SB, Marrie RA. The Impact of Psychiatric Comorbidity on Health Care Utilization in Inflammatory Bowel Disease: A Population-Based Study. Inflammatory Bowel Diseases 2021;27(9):1462-1474. 

 

IBD is associated with an increase in psychiatric comorbidity compared with the general population. We aimed to determine the impact of PC on health care utilization in persons with IBD. We applied a validated administrative definition of IBD to identify all Manitobans with IBD from April 1, 2006, to March 31, 2016, and a matched cohort without IBD. A validated definition for psychiatric comorbidity in IBD population was applied to both cohorts; active psychiatric comorbidity status meant ≥2 visits for psychiatric diagnoses within a given year. We examined the association of active psychiatric comorbidity with physician visits, inpatient hospital days, proportion with inpatient hospitalization, and use of prescription IBD medications in the following year. We tested for the presence of a 2-way interaction between cohort and PC status. Our study matched 8459 persons with IBD to 40,375 controls. On crude analysis, IBD subjects had ≥3.7 additional physician visits, had >1.5 extra hospital days, and used 2.1 more drug types annually than controls. Subjects with active psychiatric comorbidity had >10 more physician visits, had 3.1 more hospital days, and used >6.3 more drugs. There was a synergistic effect of IBD (vs no IBD) and psychiatric comorbidity (vs no psychiatric comorbidity) across psychiatric disorders of around 4%. This synergistic effect was greatest for anxiety (6% [2%, 9%]). After excluding psychiatry-related visits and psychiatry-related hospital stays, there remained an excess health care utilization in persons with IBD and PC.

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We concluded that persons with IBD with psychiatric comorbidity increases health care utilization compared with matched controls and compared with persons with IBD without psychiatric comorbidity. Active psychiatric comorbidity further increases health care utilization.

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Chhibba T, Guizzetti L, Seow CH, Lu C, Novak KL, Ananthakrishnan AN, Bernstein CN, Kaplan GG, Panaccione R, Ma C. Frequency of Opioid Prescription at Emergency Department Discharge in Patients with Inflammatory Bowel Disease: A Nationwide Analysis. Clinical Gastroenterology Hepatology 2021; 19: 2064-2071.

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Patients with IBD frequently experience chronic pain. Patients will often seek out care in the emergency department where short-term opioid use may be associated with potential treatment-related complications. We aimed to assess the rate and factors associated with opioid prescription in IBD patients discharged from the emergency department. We conducted a cross-sectional analysis of data collected in the US National Hospital Ambulatory Medical Care Survey (NHAMCS) from 2006-2017. We determined the proportion of adult patients (≥18 years) with IBD prescribed an opioid in emergency department or at emergency department discharge. We identified ∼965,000 weighted discharges from the emergency department for patients with IBD. In total, 51.9% [95% CI: 42.2% -61.6%] of visits resulted in opioid administration in the emergency department and 35.3% [95% CI: 26.5% -45.2%] of IBD-related emergency department discharges were associated with an opioid prescription. IBD patients with moderate/severe pain (adjusted odds ratio aOR 5.06 [95% CI: 1.72 -14.90], p < 0.01) were more likely to receive opioids whereas older age (aOR 0.73 per decade [95% CI: 0.55 -0.98], p = 0.04) were less likely. In temporal analysis, a trend towards decreasing opioid use in the emergency department and opioid prescriptions at discharge was observed in 2015-2017.

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More than one third of IBD patients are prescribed an opioid at discharge from the emergency department, highlighting a potential gap in care for accessing effective pain management solutions in this population.

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Banerjee R, Pal P, Nugent Z, Ganesh G, Adigopula B, Pendyala S, Bernstein CN.  IBD in India: Similar phenotype but different demographics than the West. Journal of Clinical Gastroenterology 2020; 54: 725-732.

 

Inflammatory bowel disease (IBD) is emerging in the developing world but phenotypic data are limited. In this study we aimed to describe the phenotype, clinical presentation, disease behavior and treatments of IBD in a large cohort in India. All persons presenting to the Asian Institute of Gastroenterology in Hyderabad, India since 2004 with a confirmed diagnosis of IBD were enrolled. The demographic profile at the first visit, family history of IBD, smoking history, time from first symptom onset to diagnosis, use of anti-tuberculous treatment before IBD-specific treatment, disease phenotype, and medication history were collected by interview and chart review. Disease and family history and treatments used were updated at each follow-up visit. Of 4006 persons enrolled, 59.9% had ulcerative colitis and the majority were male (60.3%). The median diagnostic delay in both ulcerative colitis and Crohn’s disease was at least two years. At the time of diagnosis only 4.5% of Crohn’s disease were smokers and only 3.8% of ulcerative colitis were ex-smokers. Positive family history was uncommon (2.1%). The phenotype of persons with Crohn’s disease included 22.9% with stricturing disease and 9.4% with fistulizing disease. The most common site of disease was ileo-colonic (40.9%) and only 2.5% had perineal fistulas. Among those with ulcerative colitis 18.7% had proctitis and 30.3% had pan-colitis.

 

This is the largest cohort of persons with IBD reported from Asia. While there are several demographic differences between persons with IBD from India compared with the West, the phenotypes of the disease are not highly different. We hope to ultimately undertake a study comparing Indians with IBD from India and Indians with IBD from Canada to contrast the differences in diet, gut microbiome and clinical presentation. This might lead us to understand causes of IBD.

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Torabi M, Bernstein CN, Yu BN, Wickramasinghe L, Blanchard JF, Singh H. Geographical variation and factors associated with inflammatory bowel disease in a central Canadian province. Inflammatory Bowel Diseases 2020; 26(4): 581-590.

 

We investigated temporal trends, geographical variation, and geographical risk factors for incidence of inflammatory bowel disease (IBD). We used the University of Manitoba IBD Epidemiology Database to identify incident IBD cases diagnosed between 1990 and 2012, which were then geocoded to 296 small geographic areas. Sociodemographic characteristics of the SGAs (proportions of immigrants, visible minorities, Indigenous people, and average household income) were obtained from the 2006 Canadian Census. The geographical variation of IBD incidence was modeled using a Bayesian spatial Poisson model. Time trends of IBD incidence were plotted using Joinpoint regression. We found that the incidence of IBD decreased over the study years from 23.6 (per 100,000 population) in 1990 to 16.3 (per 100,000 population) in 2012. For both Crohn's disease and ulcerative colitis, the highest incidence was in Winnipeg and the southern and central regions of Manitoba, whereas most of northern Manitoba had lower incidence. There was no effect of sociodemographic characteristics of small geographic areas, other than the proportion of Indigenous people, which was associated with lower IBD incidence.

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We concluded that the incidence of IBD in Manitoba is decreasing over time. We have identified geographic areas with persistently higher IBD incidence that warrant further study for etiologic clues.

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Shafer LA, Walker JR, Chhibba T, Targownik LE, Singh H, Ivekovic M, Bernstein CN. Health care indicators of moderate to severe IBD-related disability; A longitudinal study. Inflammatory Bowel Diseases 2019;25: 1996-2005.

 

We aimed to determine how health care utilization indicators in IBD that reflect moderate to severe disease relate to disability later in life. Persons in the population-based University of Manitoba IBD Research Registry completed a survey and gave permission to access their Manitoba Health records. Of 2478 people in the Registry aged 18 to 65 years, 854 participated between April 2015 and March 2016. The survey included the IBD Disability Index (IBDDI). The health data included surgeries and hospitalizations since 1984 and prescriptions since 1995. We explored the association between indicators of moderate to severe disease (ie, surgeries, hospitalization, and new corticosteroids and anti-tumor necrosis factor [anti-TNF] prescriptions) and high IBD-related disability (IBDDI greater than or 34). In addition, among those who had at least 1 IBD-related surgery, we determined predictors of low or no postsurgery disability (IBDDI less than 21). We found that 85% required at least 1 IBD-related surgery since diagnosis or had greater than 2 hospitalizations or were ever prescribed corticosteroids or anti-TNF. Surgery was more common in Crohn's disease (55%) than in UC (13%, P < 0.001). High disability was more prevalent among those ever prescribed anti-TNF (49%) vs never prescribed (28%, P < 0.001), those ever prescribed corticosteroids (35%) vs never prescribed (26%, P = 0.02), and those who had had 1 IBD-related surgery (36%) or greater than 1 surgery (53%) vs those who had had none (28%, P < 0.001).

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We concluded that health care utilization indicators of moderate to severe disease (ie, surgeries, hospitalizations, corticosteroid or anti-TNF use) were associated with subsequent higher IBD-related disability. Persons experiencing those indicators should be followed more closely for social, mental, and physical consequences of IBD-related disability. Previous health care utilization can serve as a proxy for IBD-related disability.

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Coward S, Clement F, Benchimol EI, Bernstein CN, Avina-Zubieta JA, Bitton A, Carroll MW, Hazlewood G, Jacobson K, Jelinski S, Deardon R, Jones JL, Kuenzig ME, Leddin D, McBrien KA, Murthy SK, Nguyen GC, Otley AR, Panaccione R, Rezaie A, Rosenfeld G, Peña-Sánchez JN, Singh H, Targownik LE, Kaplan GG. Past and future burden of inflammatory bowel diseases based on modeling of population-based data. Gastroenterology 2019; 156:1345-1353.

 

Inflammatory bowel diseases exist worldwide, with high prevalence in North America. IBD is complex and costly, and its increasing prevalence places a greater stress on health care systems. In this study we aimed to determine the past current, and future prevalences of IBD in Canada. We used administrative health data from Alberta (2002-2015), British Columbia (1997-2014), Manitoba (1990-2013), Nova Scotia (1996-2009), Ontario (1999-2014), Quebec (2001-2008), and Saskatchewan (1998-2016). In 2018, the prevalence of IBD in Canada was estimated at 725 per 100,000 (95% PI 716-735) and the annual average percent change increase was nearly 3% per year. The prevalence in 2030 was forecasted to be 981 per 100,000 159 per 100,000 in children, 1118 per 100,000  in adults, and 1370 per 100,000 in the elderly. In 2018, 267,983 Canadians were estimated to be living with IBD, which was forecasted to increase to 402,853 by 2030.

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Benchimol EI, Kuenzig MI, Bernstein CN, Nguyen GC, Guttmann A, Jones J, Potter BK, Targownik LE, Catley CA, Nugent Z, Tanyingoh D, Mojaverian N, Underwood FE, Siddiq S, Otley AR, Bitton A, Carroll MW, deBruyn J, Dummer TJB, El-Matary W, Griffiths AM, Jacobson K, Leddin D, Lix LM, Mack DR, Murthy SK, Peña-Sánchez JN, Singh H, Kaplan GG, on behalf of the Canadian Gastro-Intestinal Epidemiology Consortium. Rural and urban disparities in the care of Canadian patients with inflammatory bowel disease: A population-based study. Clinical Epidemiology 2018 Nov 8; 10:1613-1626.

 

Canada’s large geographic area and low population density pose challenges in access to specialized healthcare for remote and rural residents. We compared health services use, surgical rate and specialist gastroenterologist care in rural and urban IBD patients in Canada. We used validated algorithms applied to population-based health administrative data to identify all people living within 3 Canadian provinces: Alberta, Manitoba, and Ontario. We compared rural to urban residents for time to diagnosis, hospitalizations, outpatient visits, emergency department use, surgical rate, and gastroenterologist care. There were 36,656 urban and 5,223 rural residents with newly diagnosed IBD who were included. Outpatient physician visit rate was similar in rural and urban patients. IBD-specific and IBD-related hospitalization rates were higher in rural patients by 17%  and 27% (IRR 1.17, 95% CI 1.02-1.34, and IRR 1.27, 95% CI 1.04-1.56, respectively), Emergency Department in Ontario visit rate was 50% higher (IRR 1.53, 95% CI 1.42-1.65, and IRR 1.33, 95% CI 1.25-1.40) (Emergency Department visit rate could not be tracked in Alberta and Manitoba.  Surgical rates were not different between rural and urban patients, nor was pre-diagnosis lag time. Rural patients had 20% fewer IBD-specific gastroenterologist visits (IRR 0.79, 95% CI 0.73-0.84), and a smaller proportion of their IBD-specific care provided by gastroenterologists (28.3% vs. 55.2%, p<0.0001). This was less pronounced in children under age 10 at diagnosis (59.3% vs. 65.0%, p<0.0001), and the gap was widest in patients over age 65 (33.0% vs. 59.2%, p<0.0001).

 

We concluded that rural IBD patients have less use of gastroenterologists, more hospitalizations and greater rates of Emergency Department visits. These health services use disparities result in costlier care for rural patients. Innovative methods of delivering gastroenterology care to rural IBD patients (such as telehealth, online support, and/or remote clinics) should be explored, especially for communities lacking easy access to gastroenterologists.

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Ananthakrishnan A, Bernstein CN, Iliopoulos D, MacPherson A, Neurath M, Affendi RA, Vavricka S, Fiocchi C. Environmental triggers in inflammatory bowel disease: A review of progress and evidence. Nature Reviews Gastroenterology & Hepatology 2018; 15:39-49.

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This review article written by authors from around the world discusses the environmental factors that may be important in causing IBD.

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Shah SC, Khalili H, Gower-Rousseau C, Olen O, Benchimol EI, Lynge E, Nielsen KR, Brassard P, Vutcovici M, Bitton A, Bernstein CN, Leddin D, Tamim H, Stefansson T, Loftus EV, Moum B, Tang W, Ng S, Gearry R, Sincic B, Bell S, Sands BE. Lakatos PL, Végh Z, Ott C, Kaplan GG, Burisch J, Colombel JF. Sex-based difference in the incidence of inflammatory bowel disease: a pooled analysis of population-based studies. Gastroenterology 2018 Oct;155(4): 1079-1089.

 

Although the incidence of IBD varies with age, few studies have examined variations between the sexes. We therefore used population data from established cohorts to analyze sex differences in IBD incidence according to age at diagnosis. We identified population-based cohorts of patients with IBD for which incidence and age data were available (17 distinct cohorts from 16 regions of Europe, North America, Australia, and New Zealand). We collected data through December 2016 on 95,605 incident cases of Crohn's disease (42,831 male and 52,774 female) and 112,004 incident cases of UC (61,672 male and 50,332 female). We pooled incidence rate ratios of Crohn’s disease and UC for the combined cohort and compared differences according to sex using random effects meta-analysis. Female patients had a lower risk of Crohn’s disease during childhood, until the age range of 10-14 years (incidence rate ratio, 0.70; 95% CI, 0.53-0.93), but they had a higher risk of Crohn’s disease thereafter, which was statistically significant for the age groups of 25-29 years and older than 35 years. The incidence of UC did not differ significantly for female vs male patients (except for the age group of 5-9 years) until age 45 years; thereafter, men had a significantly higher incidence of UC than women.

 

We concluded that in a pooled analysis of population-based studies, we found age at IBD onset to vary with sex. Further studies are needed to investigate mechanisms of sex differences in IBD incidence.

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Melesse DY, Lix L, Nugent Z, Targownik LE, Singh H, Blanchard JF, Bernstein CN. Estimates of disease course in inflammatory bowel disease using administrative data: a population-level study. Journal of Crohn’s and Colitis 2017; 562-570.

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In this study we aimed to develop a predictive model of disease course in IBD using health care utilization measures from administrative health data. In other words we wanted to determine if we could assess administrative health data and estimate disease activity status from it. Study participants were IBD patients who were prospectively followed for a one-year period between 2009 and 2010 in a Canadian clinic setting to assess their IBD disease course (i.e., remission, mild, moderate, severe). Clinic data were linked with population-based administrative health data of Manitoba Health. We developed a statistical model to identify patters of health care utilization that matched with each disease state. The model was applied to project the distribution of disease course for the Manitoba IBD population for 1995-2013. There were 407 participants. 41% of participants were clinically in remission, while 14.0% had severe IBD. Mild, moderate, or severe disease was associated with at least 3 gastroenterologist visits or at least 3 general practitioner visits with an IBD diagnosis and at least 1 radiology test .  The percentages of the Manitoba IBD population in remission steadily rose from 1995 to 2013 (43.6% to 59.9%), while the percentages of individuals with mild, moderate or severe disease declined.

 

In summary, this study demonstrated that health care utilization measures from administrative data can be used to predict disease course in the IBD population.

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Nguyen GC, Bernstein CN, Benchimol E. Risk of surgery and mortality in elderly-onset inflammatory bowel disease: A population-based cohort study. Inflammatory Bowel Disease 2017; 23:218-223.

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In this study the administrative data of the province of Ontario was used and new IBD cases in diagnosed  between 1999 and 2008 were identified. Of 21,218 persons with IBD, there were 1749 cases of elderly-onset (at least 65 years) ulcerative colitis (UC) and 725 cases elderly-onset Crohn's disease (CD). Elderly UC had higher rates of IBD-related surgery than those with young-adult UC  (less than 40 years) (adjusted hazard ratio, 1.34; 95% CI, 1.16-1.55), although there was no difference in surgical rates between age groups in CD. IBD-specific mortality was higher in elderly-onset CD (33.1/10,000 person-year) compared with that in middle-age (40-64 years) CD (5.6/10,000 person-year, P < 0.0001) and young adult CD (1.0/10,000 person-year) but was not different by age in UC. The leading cause of death in elderly UC and CD was solid malignancies accounting for 22.9% and 26.4% of deaths, respectively, whereas IBD was third most frequent cause of death accounting for 6.3% and 9.1% of deaths, respectively. 

 

We concluded that elderly-onset patients with UC were more likely to undergo surgery while elderly-onset patients with CD exhibited higher IBD-specific death rates than those with younger-onset disease. These findings should prompt more optimized disease management in elderly IBD since they are at higher risk for bad outcomes when they are newly diagnosed.

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Benchimol EI, Kaplan GG, Otley AR, Nguyen GC, Underwood FE, Guttmann A, Jones JL, Potter BK, Catley CA, Nugent Z, Cui Y, Tanyingoh D, Mojaverian N, Bitton A, Carroll MW, deBruyn J, Dummer TJB, El-Matary W, Griffiths AM, Jacobson K, Kuenzig ME, Leddin D, Lix LM, Mack DR, Murthy S, Peña Sánchez JN, Singh H, Targownik L, Vutcovici M, Bernstein CN. Rural and urban residence during early life is associated with a lower risk of inflammatory bowel disease: A population-based inception and birth cohort study. American Journal of Gastroenterology 2017, 112:1412-1422.

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We aimed to determine if growing up in an urban or rural household impacted on being diagnosed with IBD. Using administrative data in each of 4 Canadian provinces we created comprehensive datasets of all persons with IBD in those provinces dating back to 2000.  There were 6,662 rural residents and 38,905 urban residents with IBD. The incidence of IBD per 100,000 (number of new cases) was 30.72 in rural residents and 33.16 in urban residents, (IRR 0.90, 95% CI 0.81-0.99). The protective association was strongest in children <10 years (IRR 0.58, 95% CI 0.43-0.73) and 10-17.9 years (IRR 0.72, 95% CI 0.64-0.81). In the birth cohort, comprising 331 rural and 2,302 urban residents, rurality in the first 1-5 years of life was associated with lower risk of IBD (IRR 0.75-0.78).

 

We concluded that people living in rural households had lower risk of developing IBD. This association is strongest in young children and adolescents, and in children exposed to the rural environment early in life.

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Bernstein CN. Large registry epidemiology in IBD. Inflammatory Bowel Diseases 2017;23(11):1941-1949.

 

This review article discusses the exploration of the study of the epidemiology of IBD using large databases.

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Bernstein CN. Changes in the epidemiology of inflammatory bowel disease - clues for aetiology. Alimentary Pharmacology and Therapeutics 2017;46(10):911-919.

 

This review article discusses how epidemiology studies can be used to search for clues as to what causes IBD.

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Nugent Z, Singh H, Targownik LE, Strome T, Snider C, Bernstein CN. Predictors of emergency department use by persons with IBD: A population based study. Inflammatory Bowel Diseases 2016; 22: 2907-2916.

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We aimed to describe the patterns and predictors of Emergency Department (ED) attendance and post ED hospitalization by persons with inflammatory bowel disease (IBD). We linked the University of Manitoba IBD Epidemiology Database with the Emergency Department Information System of the Winnipeg Regional Health Authority to determine the rates of presentation to the ED by persons with IBD from 01/01/09 to 03/31/12. Incident cases were diagnosed during the study period and all others were considered prevalent cases. We determined predictors of attendance in the ED and for hospitalization within 2 days of ED attendance. The study population included 300 incident and 3394 prevalent cases, of whom 76% and 49%, respectively, attended the ED at least once during the study period. Incident cases with CD (as opposed to UC) or with a history of opioid use were more likely to attend the ED. Those who had seen a gastroenterologist within the preceding year were less likely to visit the ED. Among prevalent cases higher comorbidity, opioid or corticosteroid use, and recent hospital admission were predictive of ED attendance and those who saw only one physician in the preceding year had lower ED attendance. Presenting to the ED with a primary GI complaint was the strongest predictor of subsequent hospital admission. 

 

We concluded that ED attendance by both incident and prevalent cases of IBD is high. We identified predictors of ED attendance and post ED hospitalization. This could guide the optimization of outpatient IBD care to limit ED attendance and potentially post ED hospitalization.

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Bernstein CN, Garland A, Peschken CA, Hitchon CA, Chen H, Fransoo R, Marrie RA. Predictors of ICU admission and outcomes one year post admission in persons with IBD: A population based study. Inflammatory Bowel Diseases 2015; 21: 1341-1347.

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We aimed  to determine predictors of intensive care unit (ICU) admission and to assess health care utilization post-ICU admission among persons with IBD. We matched a population-based database of Manitobans with IBD to a general population cohort by age, sex and region of residence and linked these cohorts to a population-based ICU database. We compared the incidence rates of ICU admission among prevalent IBD cases according to health care utilization (HCU) in the year prior to admission adjusting for age, sex, socioeconomic status, region, and comorbidity. Among incident cases of IBD who survived their first ICU admission we compared HCU to matched controls who survived ICU admission. Risk factors for ICU admission from the year prior to admission included cumulative corticosteroid use and IBD-related surgery. Use of immunomodulatory therapies (azathioprine, 6-mercaptopurine, and methotrexate) within one year, or surgery for IBD beyond one year prior, were not associated with ICU admission. In those who used corticosteroids and immunomodulatory medications in the year prior to ICU admission, the use of immunomodulatory medications conferred a 30% risk reduction in ICU admission. Persons with IBD who survived ICU admission had higher health care utilization in the year following ICU discharge than controls.

 

We concluded that corticosteroid use and surgery within the year are associated with ICU admission in IBD while immunomodulatory therapy is not. Surviving ICU admission is associated with high health care utilization in the year post-ICU discharge.

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Bernstein CN, Nugent ZN, Targownik LE, Singh H, Lix L. Predictors and risks for death in a population based study of persons with IBD in Manitoba. Gut 2015; 64: 1403-1411.

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We aimed to determine the predictors and risk for death among persons with either Crohn’s disease (CD) or ulcerative colitis (UC) compared to the general population.  We used the population based University of Manitoba IBD Epidemiology Database to calculate mortality rates in persons with IBD in relation to the general population. There were 10,788 prevalent cases of CD and UC and 101,860 matched controls.  Persons with CD had a 26% higher mortality rate than the general population but there was no difference in mortality for prevalent UC cases compared to matched controls. CD cases were more likely to die of colorectal cancer, non-Hodgkin lymphoma, digestive diseases, pulmonary embolism and sepsis and UC cases were more likely to die from colorectal cancer, digestive diseases, and respiratory diseases.  For incident cases there were significant effects on mortality by socioeconomic status, comorbidity score and surgery. The greatest risk for death in both CD and UC was within the first 30 days following gastrointestinal  surgery. The first year from diagnosis was also associated with increased risk of death in both CD and UC, but persisted after the 1st year only in CD.

 

We concluded that there is a significantly increased risk of mortality in CD compared to controls while in UC an increased risk for death was only evident in the first year from diagnosis. Surgery poses an increased risk for death in both CD and UC for up to 1 year.

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Marrie RA, Garland A, Peschken CA, Hitchon CA, Chen H, Fransoo R, Bernstein CN. Increased incidence of critical illness among patients with inflammatory bowel disease: A population-based study. Clinical Gastroenterology and Hepatology 2014; 12: 2063-2070.

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Little is known about intensive care unit (ICU) admission in IBD. We aimed to determine the incidence of, and mortality after ICU admission in IBD as compared to the general population, and the characteristics of critical illness (Critical illness refers to illness that leads to ICU admission) in the IBD population. We identified all persons with IBD in the province of Manitoba using a validated administrative definition of IBD for the period 1984 to 2010. Cases were considered newly diagnosed with IBD if their first health system contact for IBD was in 1989 or later. We identified a population-based control group, matched by age, sex and geography (postal code). Case and control cohorts were linked to the Manitoba ICU database containing clinical data from 93% of provincial high intensity adult ICUs. Incidence of ICU admission, reasons for ICU admission, and mortality after ICU admission were compared between groups. There were 8224 prevalent and 4580 incident cases of IBD. The risk for ICU admission was nearly twofold higher for IBD versus controls. From 2000-2010, the age and sex-standardized annual incidence of ICU admission among the prevalent IBD cohort was 0.55-1.12% (1 out of every 100 to 200 persons with IBD may get admitted to an ICU per year). Compared to controls admitted to ICUs, one year after ICU admission, mortality was increased by 32% in IBD. 

 

We concluded that in IBD there is an increased risk for ICU admission and increased mortality at one year post-ICU admission. This underscores the potential severity of IBD.

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The following series of articles was written to update the burden of IBD for Crohn’s and Colitis Canada as of the summer of 2018:

 

Benchimol E, Bernstein CN, Bitton A, Murthy SK, Nguyen GC, Lee K, Cooke-Lauder J, Siddq S, Windsor JW, Carroll M, Coward S, El-Matary W, Griffiths AM, Jones J, Kuenzig E, Lee L, Mack DR, Mawani M, Otley A, Singh H, Targownik LE, Weizman AV, Kaplan GG. The Impact of Inflammatory Bowel Disease in Canada 2018: A Scientific Report from the Canadian Gastro-Intestinal Epidemiology Consortium to Crohn's and Colitis Canada. Journal of the Canadian Association of Gastroenterology 2019; 2 Supplement 1: S1-S5.

 

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Kaplan GG, Bernstein CN, Coward S, Bitton A, Murthy SK, Nguyen GC, Lee K, Cooke-Lauder J, Benchimol E. The Impact of Inflammatory Bowel Disease in Canada 2018: Epidemiology. Journal of the Canadian Association of Gastroenterology 2019; 2 Supplement 1: S6-S16.

 

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Carroll M, Kuenzig E, Mack DR, Otley A, Griffiths AM, Kaplan GG, Bernstein CN, Bitton A, Murthy SK, Nguyen GC, Lee K, Cooke-Lauder J, Benchimol E. The Impact of Inflammatory Bowel Disease in Canada 2018: Children and Adolescents with IBD. Journal of the Canadian Association of Gastroenterology 2019; 2 Supplement 1: S49-S67.

 

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Nguyen GC, Targownik LE, Singh H, Benchimol E, Bitton A, Murthy SK, Bernstein CN, Lee K, Cooke-Lauder J, Kaplan GG. The Impact of Inflammatory Bowel Disease in Canada 2018: IBD in Seniors. Journal of the Canadian Association of Gastroenterology 2019; 2 Supplement 1: S68-S72.

 

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Bernstein CN, Benchimol E, Bitton A, Murthy SK, Nguyen GC, Lee K, Cooke-Lauder J, Kaplan GG. The Impact of Inflammatory Bowel Disease in Canada 2018: Extra-intestinal Diseases in IBD. Journal of the Canadian Association of Gastroenterology 2019; 2 Supplement 1: S73-S80.

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Rose K, Sherman PM, Cooke-Lauder J, Mawani M, Benchimol E, Kaplan GG, Bernstein CN, Bitton A, Murthy SK, Nguyen GC, Lee K. The Impact of Inflammatory Bowel Disease in Canada 2018: IBD Research Landscape in Canada. Journal of the Canadian Association of Gastroenterology 2019; 2 Supplement 1: S81-S91.

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Jones J, Nguyen GC, Benchimol E, Bernstein CN, Bitton A, Kaplan GG, Murthy SK, Lee K, Cooke-Lauder J, Otley A. The Impact of Inflammatory Bowel Disease in Canada 2018: Quality of Life. Journal of the Canadian Association of Gastroenterology. 2019; 2 Supplement 1: S42-S48.

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Keunzig ME, Lee L, El-Matary W, Weizman AV, Benchimol EI, Targownik LE, Singh H, Kaplan GG, Bernstein CN, Bitton A, Nguyen GC, Lee K, Cooke-Lauder J, Murthy S. The Impact of Inflammatory Bowel Disease in Canada 2018: Direct Costs and Health Services Utilization. Journal of the Canadian Association of Gastroenterology. 2019; 2 Supplement 1: S17-S33.

 

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Keunzig ME, Benchimol E, Lee L, Targownik LE, Singh H, Kaplan GG, Nguyen GC, Bernstein CN, Bitton A, Lee K, Cooke-Lauder J, Murthy S. The Impact of Inflammatory Bowel Disease in Canada 2018: Indirect costs of IBD care. Journal of the Canadian Association of Gastroenterology. 2019; 2 Supplement 1: S34-S41.

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