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Geographical discrepancy in oral food challenge utilization based on Canadian billing data

Geographical discrepancy in oral food challenge utilization based on Canadian billing data Background Oral food challenges (OFC) confer the highest sensitivity and specificity in diagnosis; however, uptake has been variable across clinical settings. Numerous barriers were identified in literature from inadequate training to resource access. OFC utilization patterns using billing data have not been previously studied. Objective The objective of this study is to explore the geographic differences in utilization of OFCs across Ontario and Québec using anonymized billing data from 2013 to 2017. Methods Anonymized OFC billing data were obtained between 2013 and 2017 from Ontario Health Insurance Plan (OHIP) and Régie de l’Assurance Maladie du Québec (RAMQ). The number of OFCs was extracted by location, billings, and physician demographics for clinic and hospital-based challenges. Results Over the period studied, the number of OFCs increased by 92% and 85% in Ontario clinics and Québec hospitals, respectively. For Ontario hospitals, the number of OFCs increased by 194%. While Québec performed exclusively hospital-based OFCs, after controlling for the population, the number of OFCs per 100,000 residents annually were similar to Ontario at 50 and 49 OFCs, respectively. The number of OFCs varied across the regions studied with an annual rate reaching up to 156 OFCs per 100,000 residents in urban regions and as low as 0.1 in regions furthest from city centers. Conclusion OFC utilization has steadily increased over the last decade. There has been marked geographical discrepancies in OFC utilization which could be driven by the location of allergists and heterogeneity in their practices. More research is needed to identify barriers and propose solutions to them. Keywords Oral food challenges, OFC, Food allergies, Canadian allergists, Barriers, Québec, Ontario, OHIP, RAMQ Philippe Begin and Edmond S. Chan contributed equally of Pediatrics, CHU Sainte-Justine, Montréal, QC, Canada Division of Allergy and Clinical Immunology, Department of Medicine, *Correspondence: Centre Hospitalier de l’Université de Montréal, Montréal, QC, Canada Ala El Baba Aelbaba2019@meds.uwo.ca Division of Internal Medicine, Department of Medicine, Western University, 1151 Richmond St, London, ON N6A 3K7, Canada Division of Clinical Immunology and Allergy, Department of Medicine, Western University, London, ON, Canada Division of Allergy and Immunology, Department of Pediatrics, University of British Columbia, Vancouver, BC, Canada BC Children’s Hospital Research Institute, Vancouver, BC, Canada Division of Clinical Immunology and Allergy, Department of Medicine, McMaster University, Hamilton, ON, Canada Division of Allergy, Rheumatology and Immunology, Department © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. El Baba et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 2 of 9 and 2017 was extracted from OHIP (Ontario Health Background Insurance Policy) and RAMQ (Régie de l’assurance The prevalence of food allergies (FA) is on the rise, maladie du Québec) databases which are the provincial affecting up to 9.3% of Canadians [1]. Suspected food health care systems for Ontario and Québec, respectively. allergies can lead to unnecessary food restrictions and For our study, 2017 was chosen as the end date for the anxiety surrounding accidental ingestions [2–4]. Prompt extraction of OFC billing data since Oral Immunotherapy diagnosis of FA is critical as the mainstay of treatment is (OIT) was introduced after this time and visits were identifying and eliminating allergenic foods. Currently, billed using OFC codes in Québec which would confound the diagnosis of a FA typically consists of appropriate our outcomes. The data was anonymized, and a random history, skin prick testing and serum immunoglobulin E half of the dataset was suppressed prior to extraction to levels to suspected allergens. While the objective tests ensure confidentiality [14]. confer a high sensitivity, they only have an estimated For each OFC, we extracted the age and gender of the specificity of 60% which may generate false positives ordering physician, the age and gender of the patient, the to food allergens being tested [4–6]. In contrast, oral region where the OFC was conducted, and the amount food challenges (OFC) have a sensitivity and specificity billed per OFC. OFC utilization was compared by year approaching 100% [4, 7]. and by LHINs and Administrative Regions in Ontario While OFCs are the gold standard for diagnosis, OFC and Québec, respectively. Government estimates of uptake among practitioners has been variable. Grewie population for each LHINs and Administrative Regions et al. surveyed 272 allergists in the USA, and determined in 2017 were used to calculate annual rate of OFCs per that up to 40% of eligible patients were not offered OFC 100,000 residents and expressed on heat maps for each for early peanut introduction due to barriers such as lack province. For Québec, the number of allergists with of time (69.6%), lack of staffing support (51.8%), lack of hospital positions were obtained for each administrative space to conduct OFCs (46.3%), inexperience (16.5%) and region through the province’s Plan d’Effectif Médicaux. concerns regarding hospital proximity (11.4%) [8]. Other and for Ontario, through the College of Physicians in factors that delayed OFC testing in eligible patients Ontario (CPSO) between 2013 and 2017. Descriptive included concerns over process management, lack of statistics were compiled for physician age, gender, comfort, poor reimbursement and inadequate training and speciality, for patient age and gender as well as for [9, 10]. Difference in physician compensation has also the billing fees. The association between the number been found to affect OFC utilization [11]. From a patient of OFCs and the number of allergists practising in an perspective, OFCs have been deferred as patients were administrative region was assessed with linear regression. not interested in the food item (57%), patients feared they would develop a reaction (47%), or parents feared their Results child would have a reaction (31%) [12]. In Ontario, 33,788 OFCs were performed during Finally, geographic barriers could also restrict access the study period. There were 24,423 OFCs (72.24%) to OFCs. Generally, access to specialist care in Canada performed in community clinics and 9384 (27.76%) has been limited by their shortage as well as the performed in hospital  (Additional file  1: Table  S1). distance between patients and their physicians. A recent Hospital OFCs were generally performed by younger paper published by Lee et  al. advocated for the use of physicians (average 41.0 ± 8.0 y) than those performed in telemedicine to bridge Allergy and Immunology care to community (47.2 ± 10.4y) (p < 0.00001). They were also patients with limited access in remote communities [13]. more frequently performed by female physicians (42%) Here, we hypothesize that the lack of access to OFCs compared to those performed in community setting is exacerbated by geography and corresponding deficit (34%) (OR = 1.43, p < 0.0005). in Allergist coverage. We tested this hypothesis by In Québec, 20,716 OFCs were billed during the study exploring the discrepancy in the utilization of OFCs period, all of which were performed in hospital where by geographical location as well as the trends in OFCs currently there is no billing code available for office- performed in community and hospital clinics using based challenges. Physician demographics were not anonymized large-scale billing data from two provinces available. About 51% of OFCs were billed under the in Canada. hybrid remuneration plan involving a baseline salary and partial fee-for-service whereas the rest were billed using Methods traditional fee-for-service plan. For Québec hospitals, This is a cross-sectional study that evaluated the change 61% of OFCs were performed in children younger than in OFC practice over recent years and differences 15  years old, compared to 72% in Ontario hospitals between administrative regions. Billing data on OFCs and 59% in Ontario community clinics. In the pediatric conducted in Québec and Ontario between 2013 El Baba  et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 3 of 9 Fig. 1 Oral Food Challenges in Québec and Ontario between 2013 and 2017. A, D and G present the number of oral food challenges (OFCs) performed in male (blue) vs female patients (red) according to age groups, in Québec hospitals, Ontario hospitals and Ontario clinics during the study period. B, E and H indicate the number of OFC performed for each year. C, F and I present the average number of OFCs performed per year by physicians in the two provinces. Each portion of the pie charts indicates the proportion of physicians with the various productivity. Physicians who performed an average of less than 1 OFC per year were excluded El Baba et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 4 of 9 population, 58%, 59% and 57% were performed in male The geographical difference was even more striking patients in Québec hospitals, Ontario hospitals and when considering the rate of OFCs performed per Ontario clinics, respectively, compared to 38%, 38% and 100,000 residents, annually  (Additional file  1: Table  S2 29% in the adult population (Fig.  1). In both provinces, and S3). In Ontario, Waterloo-Wellington LHIN had a there was a steady increase in the number of OFCs rate of 156 OFCs per 100,000 residents per year—well performed annually (Fig.  1). Over the 5-year period above Toronto Central and Erie St. Clair’s annual rates studied, the number of OFCs increased by 92% and 85% at 89 and 84 OFCs per 100,000 residents, respectively in Ontario clinics and Québec hospitals, respectively. (Fig.  3). When looking at the number of practicing Whereas for Ontario hospitals, the number of OFCs allergists per LHIN, Hamilton Niagara, Toronto Central almost tripled at a 194% increase. In both Québec and and Central LHINs had the most allergists at 19, 18, 18 Ontario, there was large variability in the total number of allergists each, respectively (Fig.  4). Across Ontario, OFCs performed by each physician individually, with the the average number of OFCs conducted annually per majority of OFCs being performed by less than a quarter 100,000 residents was 49 challenges. Similarly, the of allergists (Fig. 1). average number of OFCs performed annually per 100,000 In Ontario, approximately 50% of all OFCs were residents in Québec across all the administrative regions performed in 3 LHINs: Waterloo Wellington at 17.89%, was 50, with 110 OFCs performed annually per 100,000 residents in Montreal, followed by 70.6 and 69.9 OFCs in Toronto Central at 17.09% and Central at 11.49%, Laval and Capitale-Nationale, respectively (Fig. 3). When respectively. However, the most densely populated LHINs looking at the number of Allergists per Administrative were Hamilton Niagara, Central East and Champlain. Region in Québec–Montreal, Capitale-Nationale and In Québec, the majority of OFCs were performed in Montérégie had the most allergists at 37, 10 and 7 each, Montréal totalling 52.95% of the province’s OFCs (Fig 2, respectively (Fig. 4). Tables 1 and 2). Fig. 2 Heat Map demonstrating number of total OFCs conducted annually per 100,000 residents in Ontario and Québec El Baba  et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 5 of 9 Table 1 Number of OFCs performed in Ontario and performed by specialists who had hospital privileges such corresponding number of allergists and population by LHIN as pediatricians (Fig. 5). between 2013 and 2017 LHIN N of OFCs % Total population Number of allergists Discussion Using annual OFC billing data for Québec and Ontario Erie St-Clair 2746 8.12 627,633 4 from 2013 to 2017, we observed a steady increase in the South West 1866 5.52 953,261 5 uptake of OFCs within both provinces. However, we also Waterloo 6051 17.89 766,109 6 found a significant discrepancy in OFC utilization when Wellington the data was analyzed by geographic region. This finding Hamilton Niagara 3388 10.02 1,399,073 19 supports the Canadian Society of Allergy and Clinical Central West 2000 5.91 922,255 3 Immunology statement made in the context of OIT Mississauga 1973 5.83 1,164,740 12 guideline formation which describes “a situation of low Toronto central 5780 17.09 1,232,258 18 capacity and disparity in access to care for the accurate Central 3886 11.49 922,255 18 diagnosis and proper management of food allergy” [15]. Central East 1121 3.31 1,550,531 10 To the best of our knowledge, this is the first time that South East 1007 2.98 482,391 5 this disparity in access to allergy care is demonstrated Champlain 3268 9.66 1,292,639 10 in a quantitative manner using anonymized billing data, North Simcoe 421 1.24 464,406 4 Muskoka which raises significant concerns in terms of equity. North East 12 0.04 551,801 0 The heterogeneous distribution of allergists across North West 306 0.90 228,339 1 the regions studied cannot explain the geographical disparities by itself. In fact, we found that the Total 33,825 100 13,448,494 115 number of OFCs performed per year could vary by a 100-fold depending on the allergist. In Ontario, the For both Québec and Ontario, the rate of OFCs was highest absolute number of OFCs were performed strongly correlated with the number of allergists having in a Waterloo Wellington, despite having a smaller hospital privileges in the corresponding administrative population and lower number of practicing allergists regions and LHINs (R = 0.98). There were a few compared to its neighboring, densely populated LHINs administrative regions with no allergists who had OFCs such as Toronto Central and Mississauga Halton [16]. Table 2 Number of OFCs performed in Québec Hospitals and corresponding number of allergists and population by administrative region between 2013 and 2017 LHIN N of OFCs % Total population Number of allergists Bas-Saint-Laurent 138 0.67 197,385 0 Saguenay-Lac-Saint-Jean 602 2.91 276,368 0 Capitale-Nationale 2576 12.43 729,997 10 Mauricie et Centre-du-Québec 60 0.29 242,399 0 Estrie 614 2.96 319,004 4 Montréal 10,970 52.95 4,098,927 37 Outaouais 788 3.80 382,604 2 Abitibi-Témiscamingue 412 1.99 146,717 1 Côte-Nord 0 0.00 92,518 0 Nord-du-Québec 0 0.00 44,561 0 Gaspésie-Îles-de-la-Madeleine 142 0.69 90,311 0 Chaudière-Appalaches 188 0.91 420,082 1 Laval 1502 7.25 437,413 3 Lanaudière 676 3.26 494,796 3 Laurentides 172 0.83 589,400 2 Montérégie 1876 9.06 1,507,070 7 Nunavik 0 0.00 13,188 0 Terres-Cries-de-la-Baie-James 0 0.00 17,141 0 Total 20,716 100.0 8,164,361 70 El Baba et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 6 of 9 Fig. 3 Heat Map demonstrating number of clinic and hospital-based OFCs conducted annually per 100,000 residents in Ontario Interestingly, training experience has commonly been This disparity in allergists’ practice with regards to cited as a barrier to OFC performance where inadequate OFCs has a crucial implication in terms of macroscopic exposure to OFCs in fellowship limited OFC performance planning. The provincial governments’ strategy to in clinical practice [4, 9]. One of the earliest studies promote access in rural areas has been to restrict investigating OFC barriers and uptake was published practice of newly certified allergists to regions that lack by Pongracic et  al. in 2009 which showed that 45% of allergists. While this is clearly an important factor, we responding American Allergists reported never having show here that having one or many allergists does not personally performed OFCs during fellowship training guarantee that the clinical offer in OFCs will necessarily [10]. A follow-up to this study conducted by Grewie et al. follow. Qualitative studies can provide important clues in 2020 showed that in comparison to the 2009 study as to why some allergists are reluctant to offer OFCs. by Pongracic et  al. significantly more providers who This could reflect ongoing issues with resource access, performed OFCs in fellowship, offered OFCs in clinical perception of risk and reimbursement concerns which practice [18]. were all cited by American physicians as the top 3 Allergen challenges are procedures typically restricted barriers limiting their performance of office-based to Allergy and Immunology subspecialists where the OFCs [10]. These barriers were echoed in a Canadian skill is taught exclusively within Clinical Immunology study surveying allergists in British Columbia where and Allergy specialty training programs. However, given 72.6% of physicians performing OFCs reported lack the high prevalence of food and drug allergies and the of resources such as office space and support staff as influential barriers limiting OFC performance. Equally, limited number of allergists, it is currently difficult 72.6% reported that the creation of standard guidelines for allergists to manage all cases themselves. New for hospital versus community OFCs would influence interdisciplinary models need to be explored to cater to them to perform more OFCs [17]. the needs of patients with food allergies. For example, the El Baba  et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 7 of 9 Fig. 4 Heat map demonstrating the number of Allergists practicing per LHIN in Ontario and per Administrative Region in Québec administrative region with the third highest rate of OFCs OFCs, the restriction of Québec OFCs to hospitals ultimately did not limit the overall number of challenges in Québec was Saguenay-Lac-St-Jean (03) despite having completed as the number of OFCs per 100,000 residents no practicing allergists. It was also an administrative were similar in Ontario and Québec. When comparing region where OIT was successfully implemented once hospital and community based OFCs in Ontario, it was available in the province. This was made possible allergists performing OFCs in hospital were found to by pediatricians who preformed OFCs with direct access be younger and more frequently females, which may be to an allergist in Montréal who would provide clinical representative of the new generation of allergists. One direction and discuss challenging cases based on up-to- limitation here is that we cannot compare the type of date clinical practices so that patients receive specialized challenges performed in the various settings based on care despite the geographical barriers that limit their allergy severity and perceived risk. access to an allergy subspecialist locally. A little over a half of OFCs in Québec were billed The overall increase in OFC uptake likely reflects an using the hybrid remuneration plan. It is likely a increase in their demand following the recent shift in reflection that this plan is used in academic centers, practice towards a greater focus on formal diagnosis which perform most of the OFCs in the province. of food allergies, support to early introduction of Contrary to academic centers, community hospitals food allergens and threshold determination prior to often only allocate a limited number of days per month the initiation of oral immunotherapy [18, 19]. While for allergists to perform challenges and they may not technically there are two clinical settings to conducting El Baba et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 8 of 9 Conclusion In conclusion, while we observed a steady increase in the performance of OFCs across Ontario and Québec, there were major discrepancies in their clinical offer across the regions studied, irrespective of the practice setting. Addressing the various barriers to OFCs is essential, but likely insufficient on its own to ensure fair access to allergy care. The responsibility of performing OFCs will likely need to be shared in part with other practitioners in areas of limited allergist access, where allergists play a role in overseeing the transition and supporting the practice. Abbreviations OFC Oral food challenge FA Food allergies Fig. 5 Correlation between number of allergists with hospital OHIP Ontario Health Insurance Plan privileges and number of OFC performed in an administrative region RAMQ Régie de L’assurance Maladie du Québec AAAAI American Academy of Allergy, Asthma, and Immunology for the provinces of Québec and Ontario CSACI Canadian Society Allergists and Clinical Immunologists LHIN Local Health Integration Network OIT Oral immunotherapy have access to dedicated full-time nurses with the experience required to perform a large amount of Supplementary Information OFCs simultaneously. The online version contains supplementary material available at https:// doi. Limitations of our study include the generalizability org/ 10. 1186/ s13223- 022- 00751-6. of our findings as the data we collected was restricted Additional file 1: Supplementary Tables: Table S1. Demographics of to the provinces of Ontario and Québec. While all physicians performing OFCs in Ontario community and hospital clinics Canadian provinces have public healthcare models between 2013 and 2017. Table S2. Number of OFCs preformed annually funded by each of their respective provincial per 100,000 residents in Ontario Clinics and hospitals across the LHINs. Table S3. Number of OFCs preformed annually per 100,000 residents in governments, there could be regional variations in Quebec hospitals across the LHINs. the rate of food allergies, patient demographics, physician demographics and access to allergists that Acknowledgements could affect OFC utilization patterns. Moreover, Not applicable. billing codes for OFC’s could vary considerably in Author contributions different provinces [20]. Given the discrepancy in OFC AEB contributed to the literature review, data analysis and manuscript utilization we reported, future considerations include preparation. SJ contributed to the study design and manuscript preparation. the introduction of pilot projects that aim to improve PB contributed to study design, performed data extraction and curation, analysis and manuscript preparation. LS contributed to the study design and access to OFCs in LHINs and Administrative Regions manuscript preparation. Harold Kim contributed to the study design and with limited resources to perform OFCs that meet the manuscript preparation. ESC contributed to the study design and manuscript needs of their communities. In the era of telemedicine, preparation. All authors read and approved the final manuscript. allergists can utilize virtual visits to supervise low risk Funding OFCs for patients who have an epinephrine device at BC Children’s Foundation and Fonds de Recherche du Québec – Santé home and who understand the signs and symptoms of (281662). a reaction and when to treat [21]. Such initiatives could Availability of data and materials also be expanded to virtually connect community The data that support the findings of this study are available from OHIP and pediatricians or internists to allergists from academic RAMQ. Restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. centers to direct higher risk in-office OFCs in order to increase their utilization and improve equity in Declarations management of food allergies, which are on the rise (Additional file 1). Ethics approval and consent to participate Not applicable. Consent for publication Not applicable. El Baba  et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 9 of 9 Competing interests 17. Hsu E, Soller L, Abrams EM, Protudjer JLP, Mill C, Chan ES. Oral food Dr. Ala El Baba declares that they have no competing interests. Dr. Lianne challenge implementation: the first mixed-methods study exploring Soller declares that they have no competing interests. Dr. Edmond Chan has barriers and solutions. J Allergy Clin Immunol Pract. 2020;8(1):149-156.e1. received research support from DBV Technologies; and has been a member 18. Greiwe J, Oppenheimer J, Bird JA, Fleischer DM, Pongracic JA, Greenhawt of advisory boards for Pfizer, Pediapharm, Leo Pharma, Kaleo, DBV, AllerGenis, M. AAAAI work group report: trends in oral food challenge practices Sanofi Genzyme, Bausch Health, Avir Pharma. Dr. Philip Bégin has received among allergists in the United States. J Allergy Clin Immunol Pract. research support from DBV Technologies, Novartis, Sanofi and Regeneron; and 2020;8(10):3348–55. has been a member of advisory boards/speaker’s bureau for Pfizer, DBV, Sanofi 19. Graham F, Mack DP, Bégin P. Practical challenges in oral immunotherapy Genzyme, Bausch Health, Novartis, Aralez and ALK. Dr. Samira Jeimy has been resolved through patient-centered care. Allergy Asthma Clin Immunol. on speaker’s bureaus for Aralez, AstraZeneca, GSK, Sanofi, and Novartis, and on 2021;17(1):31–31. advisory boards for Sanofi and Aralez. Dr. Harold Kim has served on speakers’ 20. Protudjer JLP, Soller L, Abrams EM, Chan ES. Billing fees for various bureau and/or advisory boards: AstraZeneca, Aralez, Bausch Health, CSL common allergy tests vary widely across Canada. Allergy Asthma Clin Behring, GSK, Kaleo, Novartis, Pediapharm, Pfizer, Sanofi, Shire, Takeda. Immunol. 2020;16(1):28–28. 21. Mack DP, Chan ES, Shaker M, Abrams EM, Wang J, Fleischer DM, et al. Novel approaches to food allergy management during COVID-19 inspire Received: 9 November 2022 Accepted: 8 December 2022 long-term change. J Allergy Clin Immunol Pract. 2020;8(9):2851–7. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. References 1. 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Geographical discrepancy in oral food challenge utilization based on Canadian billing data

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Abstract

Background Oral food challenges (OFC) confer the highest sensitivity and specificity in diagnosis; however, uptake has been variable across clinical settings. Numerous barriers were identified in literature from inadequate training to resource access. OFC utilization patterns using billing data have not been previously studied. Objective The objective of this study is to explore the geographic differences in utilization of OFCs across Ontario and Québec using anonymized billing data from 2013 to 2017. Methods Anonymized OFC billing data were obtained between 2013 and 2017 from Ontario Health Insurance Plan (OHIP) and Régie de l’Assurance Maladie du Québec (RAMQ). The number of OFCs was extracted by location, billings, and physician demographics for clinic and hospital-based challenges. Results Over the period studied, the number of OFCs increased by 92% and 85% in Ontario clinics and Québec hospitals, respectively. For Ontario hospitals, the number of OFCs increased by 194%. While Québec performed exclusively hospital-based OFCs, after controlling for the population, the number of OFCs per 100,000 residents annually were similar to Ontario at 50 and 49 OFCs, respectively. The number of OFCs varied across the regions studied with an annual rate reaching up to 156 OFCs per 100,000 residents in urban regions and as low as 0.1 in regions furthest from city centers. Conclusion OFC utilization has steadily increased over the last decade. There has been marked geographical discrepancies in OFC utilization which could be driven by the location of allergists and heterogeneity in their practices. More research is needed to identify barriers and propose solutions to them. Keywords Oral food challenges, OFC, Food allergies, Canadian allergists, Barriers, Québec, Ontario, OHIP, RAMQ Philippe Begin and Edmond S. Chan contributed equally of Pediatrics, CHU Sainte-Justine, Montréal, QC, Canada Division of Allergy and Clinical Immunology, Department of Medicine, *Correspondence: Centre Hospitalier de l’Université de Montréal, Montréal, QC, Canada Ala El Baba Aelbaba2019@meds.uwo.ca Division of Internal Medicine, Department of Medicine, Western University, 1151 Richmond St, London, ON N6A 3K7, Canada Division of Clinical Immunology and Allergy, Department of Medicine, Western University, London, ON, Canada Division of Allergy and Immunology, Department of Pediatrics, University of British Columbia, Vancouver, BC, Canada BC Children’s Hospital Research Institute, Vancouver, BC, Canada Division of Clinical Immunology and Allergy, Department of Medicine, McMaster University, Hamilton, ON, Canada Division of Allergy, Rheumatology and Immunology, Department © The Author(s) 2023. 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The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. El Baba et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 2 of 9 and 2017 was extracted from OHIP (Ontario Health Background Insurance Policy) and RAMQ (Régie de l’assurance The prevalence of food allergies (FA) is on the rise, maladie du Québec) databases which are the provincial affecting up to 9.3% of Canadians [1]. Suspected food health care systems for Ontario and Québec, respectively. allergies can lead to unnecessary food restrictions and For our study, 2017 was chosen as the end date for the anxiety surrounding accidental ingestions [2–4]. Prompt extraction of OFC billing data since Oral Immunotherapy diagnosis of FA is critical as the mainstay of treatment is (OIT) was introduced after this time and visits were identifying and eliminating allergenic foods. Currently, billed using OFC codes in Québec which would confound the diagnosis of a FA typically consists of appropriate our outcomes. The data was anonymized, and a random history, skin prick testing and serum immunoglobulin E half of the dataset was suppressed prior to extraction to levels to suspected allergens. While the objective tests ensure confidentiality [14]. confer a high sensitivity, they only have an estimated For each OFC, we extracted the age and gender of the specificity of 60% which may generate false positives ordering physician, the age and gender of the patient, the to food allergens being tested [4–6]. In contrast, oral region where the OFC was conducted, and the amount food challenges (OFC) have a sensitivity and specificity billed per OFC. OFC utilization was compared by year approaching 100% [4, 7]. and by LHINs and Administrative Regions in Ontario While OFCs are the gold standard for diagnosis, OFC and Québec, respectively. Government estimates of uptake among practitioners has been variable. Grewie population for each LHINs and Administrative Regions et al. surveyed 272 allergists in the USA, and determined in 2017 were used to calculate annual rate of OFCs per that up to 40% of eligible patients were not offered OFC 100,000 residents and expressed on heat maps for each for early peanut introduction due to barriers such as lack province. For Québec, the number of allergists with of time (69.6%), lack of staffing support (51.8%), lack of hospital positions were obtained for each administrative space to conduct OFCs (46.3%), inexperience (16.5%) and region through the province’s Plan d’Effectif Médicaux. concerns regarding hospital proximity (11.4%) [8]. Other and for Ontario, through the College of Physicians in factors that delayed OFC testing in eligible patients Ontario (CPSO) between 2013 and 2017. Descriptive included concerns over process management, lack of statistics were compiled for physician age, gender, comfort, poor reimbursement and inadequate training and speciality, for patient age and gender as well as for [9, 10]. Difference in physician compensation has also the billing fees. The association between the number been found to affect OFC utilization [11]. From a patient of OFCs and the number of allergists practising in an perspective, OFCs have been deferred as patients were administrative region was assessed with linear regression. not interested in the food item (57%), patients feared they would develop a reaction (47%), or parents feared their Results child would have a reaction (31%) [12]. In Ontario, 33,788 OFCs were performed during Finally, geographic barriers could also restrict access the study period. There were 24,423 OFCs (72.24%) to OFCs. Generally, access to specialist care in Canada performed in community clinics and 9384 (27.76%) has been limited by their shortage as well as the performed in hospital  (Additional file  1: Table  S1). distance between patients and their physicians. A recent Hospital OFCs were generally performed by younger paper published by Lee et  al. advocated for the use of physicians (average 41.0 ± 8.0 y) than those performed in telemedicine to bridge Allergy and Immunology care to community (47.2 ± 10.4y) (p < 0.00001). They were also patients with limited access in remote communities [13]. more frequently performed by female physicians (42%) Here, we hypothesize that the lack of access to OFCs compared to those performed in community setting is exacerbated by geography and corresponding deficit (34%) (OR = 1.43, p < 0.0005). in Allergist coverage. We tested this hypothesis by In Québec, 20,716 OFCs were billed during the study exploring the discrepancy in the utilization of OFCs period, all of which were performed in hospital where by geographical location as well as the trends in OFCs currently there is no billing code available for office- performed in community and hospital clinics using based challenges. Physician demographics were not anonymized large-scale billing data from two provinces available. About 51% of OFCs were billed under the in Canada. hybrid remuneration plan involving a baseline salary and partial fee-for-service whereas the rest were billed using Methods traditional fee-for-service plan. For Québec hospitals, This is a cross-sectional study that evaluated the change 61% of OFCs were performed in children younger than in OFC practice over recent years and differences 15  years old, compared to 72% in Ontario hospitals between administrative regions. Billing data on OFCs and 59% in Ontario community clinics. In the pediatric conducted in Québec and Ontario between 2013 El Baba  et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 3 of 9 Fig. 1 Oral Food Challenges in Québec and Ontario between 2013 and 2017. A, D and G present the number of oral food challenges (OFCs) performed in male (blue) vs female patients (red) according to age groups, in Québec hospitals, Ontario hospitals and Ontario clinics during the study period. B, E and H indicate the number of OFC performed for each year. C, F and I present the average number of OFCs performed per year by physicians in the two provinces. Each portion of the pie charts indicates the proportion of physicians with the various productivity. Physicians who performed an average of less than 1 OFC per year were excluded El Baba et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 4 of 9 population, 58%, 59% and 57% were performed in male The geographical difference was even more striking patients in Québec hospitals, Ontario hospitals and when considering the rate of OFCs performed per Ontario clinics, respectively, compared to 38%, 38% and 100,000 residents, annually  (Additional file  1: Table  S2 29% in the adult population (Fig.  1). In both provinces, and S3). In Ontario, Waterloo-Wellington LHIN had a there was a steady increase in the number of OFCs rate of 156 OFCs per 100,000 residents per year—well performed annually (Fig.  1). Over the 5-year period above Toronto Central and Erie St. Clair’s annual rates studied, the number of OFCs increased by 92% and 85% at 89 and 84 OFCs per 100,000 residents, respectively in Ontario clinics and Québec hospitals, respectively. (Fig.  3). When looking at the number of practicing Whereas for Ontario hospitals, the number of OFCs allergists per LHIN, Hamilton Niagara, Toronto Central almost tripled at a 194% increase. In both Québec and and Central LHINs had the most allergists at 19, 18, 18 Ontario, there was large variability in the total number of allergists each, respectively (Fig.  4). Across Ontario, OFCs performed by each physician individually, with the the average number of OFCs conducted annually per majority of OFCs being performed by less than a quarter 100,000 residents was 49 challenges. Similarly, the of allergists (Fig. 1). average number of OFCs performed annually per 100,000 In Ontario, approximately 50% of all OFCs were residents in Québec across all the administrative regions performed in 3 LHINs: Waterloo Wellington at 17.89%, was 50, with 110 OFCs performed annually per 100,000 residents in Montreal, followed by 70.6 and 69.9 OFCs in Toronto Central at 17.09% and Central at 11.49%, Laval and Capitale-Nationale, respectively (Fig. 3). When respectively. However, the most densely populated LHINs looking at the number of Allergists per Administrative were Hamilton Niagara, Central East and Champlain. Region in Québec–Montreal, Capitale-Nationale and In Québec, the majority of OFCs were performed in Montérégie had the most allergists at 37, 10 and 7 each, Montréal totalling 52.95% of the province’s OFCs (Fig 2, respectively (Fig. 4). Tables 1 and 2). Fig. 2 Heat Map demonstrating number of total OFCs conducted annually per 100,000 residents in Ontario and Québec El Baba  et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 5 of 9 Table 1 Number of OFCs performed in Ontario and performed by specialists who had hospital privileges such corresponding number of allergists and population by LHIN as pediatricians (Fig. 5). between 2013 and 2017 LHIN N of OFCs % Total population Number of allergists Discussion Using annual OFC billing data for Québec and Ontario Erie St-Clair 2746 8.12 627,633 4 from 2013 to 2017, we observed a steady increase in the South West 1866 5.52 953,261 5 uptake of OFCs within both provinces. However, we also Waterloo 6051 17.89 766,109 6 found a significant discrepancy in OFC utilization when Wellington the data was analyzed by geographic region. This finding Hamilton Niagara 3388 10.02 1,399,073 19 supports the Canadian Society of Allergy and Clinical Central West 2000 5.91 922,255 3 Immunology statement made in the context of OIT Mississauga 1973 5.83 1,164,740 12 guideline formation which describes “a situation of low Toronto central 5780 17.09 1,232,258 18 capacity and disparity in access to care for the accurate Central 3886 11.49 922,255 18 diagnosis and proper management of food allergy” [15]. Central East 1121 3.31 1,550,531 10 To the best of our knowledge, this is the first time that South East 1007 2.98 482,391 5 this disparity in access to allergy care is demonstrated Champlain 3268 9.66 1,292,639 10 in a quantitative manner using anonymized billing data, North Simcoe 421 1.24 464,406 4 Muskoka which raises significant concerns in terms of equity. North East 12 0.04 551,801 0 The heterogeneous distribution of allergists across North West 306 0.90 228,339 1 the regions studied cannot explain the geographical disparities by itself. In fact, we found that the Total 33,825 100 13,448,494 115 number of OFCs performed per year could vary by a 100-fold depending on the allergist. In Ontario, the For both Québec and Ontario, the rate of OFCs was highest absolute number of OFCs were performed strongly correlated with the number of allergists having in a Waterloo Wellington, despite having a smaller hospital privileges in the corresponding administrative population and lower number of practicing allergists regions and LHINs (R = 0.98). There were a few compared to its neighboring, densely populated LHINs administrative regions with no allergists who had OFCs such as Toronto Central and Mississauga Halton [16]. Table 2 Number of OFCs performed in Québec Hospitals and corresponding number of allergists and population by administrative region between 2013 and 2017 LHIN N of OFCs % Total population Number of allergists Bas-Saint-Laurent 138 0.67 197,385 0 Saguenay-Lac-Saint-Jean 602 2.91 276,368 0 Capitale-Nationale 2576 12.43 729,997 10 Mauricie et Centre-du-Québec 60 0.29 242,399 0 Estrie 614 2.96 319,004 4 Montréal 10,970 52.95 4,098,927 37 Outaouais 788 3.80 382,604 2 Abitibi-Témiscamingue 412 1.99 146,717 1 Côte-Nord 0 0.00 92,518 0 Nord-du-Québec 0 0.00 44,561 0 Gaspésie-Îles-de-la-Madeleine 142 0.69 90,311 0 Chaudière-Appalaches 188 0.91 420,082 1 Laval 1502 7.25 437,413 3 Lanaudière 676 3.26 494,796 3 Laurentides 172 0.83 589,400 2 Montérégie 1876 9.06 1,507,070 7 Nunavik 0 0.00 13,188 0 Terres-Cries-de-la-Baie-James 0 0.00 17,141 0 Total 20,716 100.0 8,164,361 70 El Baba et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 6 of 9 Fig. 3 Heat Map demonstrating number of clinic and hospital-based OFCs conducted annually per 100,000 residents in Ontario Interestingly, training experience has commonly been This disparity in allergists’ practice with regards to cited as a barrier to OFC performance where inadequate OFCs has a crucial implication in terms of macroscopic exposure to OFCs in fellowship limited OFC performance planning. The provincial governments’ strategy to in clinical practice [4, 9]. One of the earliest studies promote access in rural areas has been to restrict investigating OFC barriers and uptake was published practice of newly certified allergists to regions that lack by Pongracic et  al. in 2009 which showed that 45% of allergists. While this is clearly an important factor, we responding American Allergists reported never having show here that having one or many allergists does not personally performed OFCs during fellowship training guarantee that the clinical offer in OFCs will necessarily [10]. A follow-up to this study conducted by Grewie et al. follow. Qualitative studies can provide important clues in 2020 showed that in comparison to the 2009 study as to why some allergists are reluctant to offer OFCs. by Pongracic et  al. significantly more providers who This could reflect ongoing issues with resource access, performed OFCs in fellowship, offered OFCs in clinical perception of risk and reimbursement concerns which practice [18]. were all cited by American physicians as the top 3 Allergen challenges are procedures typically restricted barriers limiting their performance of office-based to Allergy and Immunology subspecialists where the OFCs [10]. These barriers were echoed in a Canadian skill is taught exclusively within Clinical Immunology study surveying allergists in British Columbia where and Allergy specialty training programs. However, given 72.6% of physicians performing OFCs reported lack the high prevalence of food and drug allergies and the of resources such as office space and support staff as influential barriers limiting OFC performance. Equally, limited number of allergists, it is currently difficult 72.6% reported that the creation of standard guidelines for allergists to manage all cases themselves. New for hospital versus community OFCs would influence interdisciplinary models need to be explored to cater to them to perform more OFCs [17]. the needs of patients with food allergies. For example, the El Baba  et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 7 of 9 Fig. 4 Heat map demonstrating the number of Allergists practicing per LHIN in Ontario and per Administrative Region in Québec administrative region with the third highest rate of OFCs OFCs, the restriction of Québec OFCs to hospitals ultimately did not limit the overall number of challenges in Québec was Saguenay-Lac-St-Jean (03) despite having completed as the number of OFCs per 100,000 residents no practicing allergists. It was also an administrative were similar in Ontario and Québec. When comparing region where OIT was successfully implemented once hospital and community based OFCs in Ontario, it was available in the province. This was made possible allergists performing OFCs in hospital were found to by pediatricians who preformed OFCs with direct access be younger and more frequently females, which may be to an allergist in Montréal who would provide clinical representative of the new generation of allergists. One direction and discuss challenging cases based on up-to- limitation here is that we cannot compare the type of date clinical practices so that patients receive specialized challenges performed in the various settings based on care despite the geographical barriers that limit their allergy severity and perceived risk. access to an allergy subspecialist locally. A little over a half of OFCs in Québec were billed The overall increase in OFC uptake likely reflects an using the hybrid remuneration plan. It is likely a increase in their demand following the recent shift in reflection that this plan is used in academic centers, practice towards a greater focus on formal diagnosis which perform most of the OFCs in the province. of food allergies, support to early introduction of Contrary to academic centers, community hospitals food allergens and threshold determination prior to often only allocate a limited number of days per month the initiation of oral immunotherapy [18, 19]. While for allergists to perform challenges and they may not technically there are two clinical settings to conducting El Baba et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 8 of 9 Conclusion In conclusion, while we observed a steady increase in the performance of OFCs across Ontario and Québec, there were major discrepancies in their clinical offer across the regions studied, irrespective of the practice setting. Addressing the various barriers to OFCs is essential, but likely insufficient on its own to ensure fair access to allergy care. The responsibility of performing OFCs will likely need to be shared in part with other practitioners in areas of limited allergist access, where allergists play a role in overseeing the transition and supporting the practice. Abbreviations OFC Oral food challenge FA Food allergies Fig. 5 Correlation between number of allergists with hospital OHIP Ontario Health Insurance Plan privileges and number of OFC performed in an administrative region RAMQ Régie de L’assurance Maladie du Québec AAAAI American Academy of Allergy, Asthma, and Immunology for the provinces of Québec and Ontario CSACI Canadian Society Allergists and Clinical Immunologists LHIN Local Health Integration Network OIT Oral immunotherapy have access to dedicated full-time nurses with the experience required to perform a large amount of Supplementary Information OFCs simultaneously. The online version contains supplementary material available at https:// doi. Limitations of our study include the generalizability org/ 10. 1186/ s13223- 022- 00751-6. of our findings as the data we collected was restricted Additional file 1: Supplementary Tables: Table S1. Demographics of to the provinces of Ontario and Québec. While all physicians performing OFCs in Ontario community and hospital clinics Canadian provinces have public healthcare models between 2013 and 2017. Table S2. Number of OFCs preformed annually funded by each of their respective provincial per 100,000 residents in Ontario Clinics and hospitals across the LHINs. Table S3. Number of OFCs preformed annually per 100,000 residents in governments, there could be regional variations in Quebec hospitals across the LHINs. the rate of food allergies, patient demographics, physician demographics and access to allergists that Acknowledgements could affect OFC utilization patterns. Moreover, Not applicable. billing codes for OFC’s could vary considerably in Author contributions different provinces [20]. Given the discrepancy in OFC AEB contributed to the literature review, data analysis and manuscript utilization we reported, future considerations include preparation. SJ contributed to the study design and manuscript preparation. the introduction of pilot projects that aim to improve PB contributed to study design, performed data extraction and curation, analysis and manuscript preparation. LS contributed to the study design and access to OFCs in LHINs and Administrative Regions manuscript preparation. Harold Kim contributed to the study design and with limited resources to perform OFCs that meet the manuscript preparation. ESC contributed to the study design and manuscript needs of their communities. In the era of telemedicine, preparation. All authors read and approved the final manuscript. allergists can utilize virtual visits to supervise low risk Funding OFCs for patients who have an epinephrine device at BC Children’s Foundation and Fonds de Recherche du Québec – Santé home and who understand the signs and symptoms of (281662). a reaction and when to treat [21]. Such initiatives could Availability of data and materials also be expanded to virtually connect community The data that support the findings of this study are available from OHIP and pediatricians or internists to allergists from academic RAMQ. Restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. centers to direct higher risk in-office OFCs in order to increase their utilization and improve equity in Declarations management of food allergies, which are on the rise (Additional file 1). Ethics approval and consent to participate Not applicable. Consent for publication Not applicable. El Baba  et al. Allergy, Asthma & Clinical Immunology (2023) 19:5 Page 9 of 9 Competing interests 17. Hsu E, Soller L, Abrams EM, Protudjer JLP, Mill C, Chan ES. Oral food Dr. Ala El Baba declares that they have no competing interests. Dr. Lianne challenge implementation: the first mixed-methods study exploring Soller declares that they have no competing interests. Dr. Edmond Chan has barriers and solutions. J Allergy Clin Immunol Pract. 2020;8(1):149-156.e1. received research support from DBV Technologies; and has been a member 18. Greiwe J, Oppenheimer J, Bird JA, Fleischer DM, Pongracic JA, Greenhawt of advisory boards for Pfizer, Pediapharm, Leo Pharma, Kaleo, DBV, AllerGenis, M. AAAAI work group report: trends in oral food challenge practices Sanofi Genzyme, Bausch Health, Avir Pharma. Dr. Philip Bégin has received among allergists in the United States. J Allergy Clin Immunol Pract. research support from DBV Technologies, Novartis, Sanofi and Regeneron; and 2020;8(10):3348–55. has been a member of advisory boards/speaker’s bureau for Pfizer, DBV, Sanofi 19. Graham F, Mack DP, Bégin P. Practical challenges in oral immunotherapy Genzyme, Bausch Health, Novartis, Aralez and ALK. Dr. Samira Jeimy has been resolved through patient-centered care. Allergy Asthma Clin Immunol. on speaker’s bureaus for Aralez, AstraZeneca, GSK, Sanofi, and Novartis, and on 2021;17(1):31–31. advisory boards for Sanofi and Aralez. Dr. Harold Kim has served on speakers’ 20. Protudjer JLP, Soller L, Abrams EM, Chan ES. Billing fees for various bureau and/or advisory boards: AstraZeneca, Aralez, Bausch Health, CSL common allergy tests vary widely across Canada. Allergy Asthma Clin Behring, GSK, Kaleo, Novartis, Pediapharm, Pfizer, Sanofi, Shire, Takeda. Immunol. 2020;16(1):28–28. 21. Mack DP, Chan ES, Shaker M, Abrams EM, Wang J, Fleischer DM, et al. Novel approaches to food allergy management during COVID-19 inspire Received: 9 November 2022 Accepted: 8 December 2022 long-term change. J Allergy Clin Immunol Pract. 2020;8(9):2851–7. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. References 1. 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Journal

"Allergy, Asthma & Clinical Immunology" – Springer Journals

Published: Jan 17, 2023

Keywords: Oral food challenges; OFC; Food allergies; Canadian allergists; Barriers; Québec; Ontario; OHIP; RAMQ

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