The feasibility of an allergy management support system (AMSS) for IgE-mediated allergy in primary care

The feasibility of an allergy management support system (AMSS) for IgE-mediated allergy in... Background: The allergy management support system (AMSS) was developed to assist general practitioners (GPs) to handle the increasing burden of allergic diseases and facilitates the diagnosis and management of allergy. The aim of this cluster‑ randomized controlled pilot study was to test the feasibility of this AMSS for primary care. Methods: GPs received diagnostic and management recommendations generated by the AMSS in addition to sIgE‑ test results (intervention) or GPs received sIgE‑ test results only (control). The AMSS recommendations are based on the previously developed patient‑ completed AMSS questionnaire and sIgE‑ test results. The AMSS was considered feasible when > 70% of the AMSS recommendations were sent to the GP within ten working days of sIgE‑ testing. GPs completed a questionnaire on their diagnosis and management before ( T1) and after ( T2) receiving sIgE test results. Agreement and disagreement concerning diagnosis, medication and referrals between GPs and AMSS was investi‑ gated at T1 and T2. A total agreement score between GPs and AMSS was calculated. GPs in the intervention group completed a questionnaire to evaluate the utility of the AMSS. Semi‑ structured interviews were used to explore the motivation of GPs who did not include patients in this pilot study. Results: Twenty‑ seven GPs included 101 patients. Forty‑ two patients (72%) completed the AMSS questionnaire in the intervention group. The majority of the AMSS recommendations (93%) were returned to the GP within 10 working days after sIgE‑ test results were known [mean (SD) 4.7 (4.0) working days]. GPs in the intervention group reported largely following the AMSS recommendations in 71% of cases. The total agreement scores concerning diagnosis were significantly higher (p < 0.001) in the intervention group than the control group [mean (SD); 0.9 (1.8) vs − 0.8 (1.0)]. The agreement concerning medication or referral between GPs and AMSS did not differ between the intervention and the control group. GPs in the intervention group were reasonably positive about the AMSS. Not enrolling patients was not caused by anticipated ineffectiveness of the AMSS. Conclusion: The AMSS can be considered to be feasible for primary care. GPs tend to follow the AMSS recommenda‑ tions. The AMSS may contribute to the empowerment of GPs to better manage allergy patients in primary care. Trial registration ISRCTN ISRCTN36780877. Registered 23 November 2017 (retrospectively registered) Keywords: Allergy, Diagnosis, Feasibility, Management support system, Primary care *Correspondence: b.m.j.flokstra@umcg.nl University of Groningen, University Medical Center Groningen, Department of General Practice, Internal Postcode FA21, PO Box 196, 9700 AD Groningen, The Netherlands Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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. Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 2 of 10 results only. GPs included patients in the study during Background a 6-month period (from January 2014 until July 2014). Allergy is one of the most common chronic diseases with This pilot study was approved by the local medical ethics the number of people suffering from allergic diseases committee (METc 2013/129) who deemed that the study increasing worldwide [1–4]. Currently, more than 150 did not fall within the Dutch Medical Research Involv- million people in Europe experience allergic symptoms ing Human Subjects Act. Participation was voluntary, all [5]. The number of certified allergists per head of popu - participants received written information about the study lation ranges from 1:1,240,000 to 1:16,000 in European and all participants signed an informed consent form. countries [6]. About 50% of all children under 18  years visit their general practitioner (GP) for allergic symptoms [7]. Diagnosis and management of patients suspected of Participants allergy is often performed by GPs. In many cases, espe- All GPs allied to a single regional GP laboratory in the cially where there are very few allergists operating in northern part of the Netherlands were invited to partici- large populations, GPs are exclusively responsible for pate in this pilot study. The practices of GPs that agreed providing allergy care [8]. to participate were randomized to the intervention or GPs report having difficulties in diagnosing and man - the control group. The GPs included eligible patients aging allergic patients, including the interpretation (both children and adults). The only inclusion criterion of specific IgE (sIgE), which they attribute to a lack of was that the GP had ordered a sIgE test (usually screen- allergy training [9]. Of the major allergic diseases, food ing of inhalant allergens (grass pollen, tree pollen, house allergy has been reported by GPs as the most trouble- dust mite, cat, dog, moulds, weed pollen) or food aller- some [10, 11]. In addition, it has been shown that of the gens (hen’s egg, milk, cod, wheat, peanut, soy) for that case mix of patients referred to a regional allergy service particular patient regarding an allergy related problem. by GPs, only 43% of patients were diagnosed with an IgE There were no explicit exclusion criteria. A formal power mediated allergic disease [12]. In the United Kingdom, it calculation was not applicable, since this is a pilot study has been reported that probably a quarter and maybe half which aims to investigate the feasibility of the AMSS for of allergy referrals to secondary care may be dealt with primary care. in primary care by a GP with special interest in allergy [13]. These results demonstrate that allergy management The allergy management support system (AMSS) in primary care is not optimal in most European coun- Participating patients in the intervention and control tries [14]. group completed the AMSS questionnaire and sent Since the specialist-based allergy care model will the questionnaire to the AMSS researchers for analy- become unsustainable with increasing allergy preva- sis together with the sIgE test results. Previously devel- lence, a new allergy care model with a more important oped algorithms (for adults and children) were used to role for the GP is mandatory [8]. Therefore, we devel - allocate patients to predefined diagnostic categories and oped an allergy management support system (AMSS) to consequent recommendations for management [15]. support GPs in diagnosing and managing patients with In addition, the AMSS questionnaire, sIgE test results IgE-mediated allergy in primary care [11, 15]. Based on and resultant AMSS recommendations were checked a patient-reported history questionnaire and specific IgE by allergy specialists for inaccuracies or ambiguities. An (sIgE) blood test results, we could demonstrate that the AMSS advice was formulated for patients in the interven- AMSS is able to provide a probable diagnosis and recom- tion and control group. The AMSS recommendations, mendations on management of allergic disorders for GPs together with a copy of the completed AMSS question- [15]. The primary aim of this pilot study was to test the naire and the sIgE test outcome, were sent only to the feasibility of an AMSS for primary care. In addition, pre- GPs in the intervention group by post (Fig. 1). The AMSS liminary effects of the AMSS on diagnosis, medication recommendations formulated for patients in the control and referrals were investigated. Finally, an evaluation of group were for evaluative purposes only and were not the AMSS by the GPs was carried out. made available to the GPs in the control group. Methods Measures in patients Study design Participating patients in the intervention and control Using a cluster randomized controlled design, GPs in group completed the AMSS questionnaire which consists the intervention group received AMSS recommenda- of 12 (mainly) multiple-choice questions on symptoms, tions in addition to sIgE test results, while GPs in the triggers, severity, medication and symptom control of control group performed usual care based on sIgE test their allergic condition(s) [15]. Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 3 of 10 the AMSS for primary care. This questionnaire consisted of 13 multiple-choice questions and one question to rate the AMSS system with a score between 1 (worst) and 10 (best). Qualitative evaluation After the inclusion period, it turned out that 27 (36%) of the 75 GPs included patients in the study. Qualita- tive research was undertaken to eliminate possible (self ) selection bias and ascertain the generalizability of the results. Semi-structured interviews were used to explore the motivation of GPs who did not include patients in the pilot study. In order to obtain diversity in the qualita- tive sample, GPs were purposively selected based on the allocation of the GP to the intervention or control group, sex of the GP and location of the GP’s practice. GPs were interviewed until saturation was reached. Interviews were transcribed verbatim and analyzed using Atlas.ti based on the grounded theory [16, 17]. Statistical analysis The AMSS was considered feasible if > 70% of the AMSS recommendations was sent to the GP within 10 working days of sIgE testing. Descriptive statistics included mean (SD) and percentages. Non-parametric statistics were Fig. 1 Schematic representation of the allergy management support performed using Mann–Whitney U test or Fisher exact system (AMSS) [15] test. Agreement and disagreement concerning diagnosis, medication and referrals between GPs and AMSS were investigated at T1 and T2. For each patient, agreement was the number of diagnoses made by both the AMSS Measures in GPs and the GP. There were two types of disagreement: the Efficacy measure and case‑specific evaluation first was the number of diagnoses made by the AMSS but GPs in both groups completed a short questionnaire with not by the GP (referred to hereafter as disagreement A) multiple-choice questions on diagnosis and management and the second was the number of diagnoses made by the (medication, referral and/or non-pharmacotherapeutic GP but not by the AMSS (disagreement B). A total agree- recommendations). This questionnaire was completed ment score was then calculated as agreement minus both on two occasions: at the time of inclusion of the patient disagreement A and B. Finally, the change of the scores (T1) and at the time the sIgE test outcomes (and in the were calculated as T2 scores minus T1 scores. The same case of the intervention group, the AMSS recommenda- methodology was used for (dis)agreement concerning tions) were known (T2). In addition, the T2 question- medication prescriptions and referrals. The data was ana - naire included a question on the GPs’ satisfaction with lysed using SPSS22.0 (IBM, Chicago, USA). their own management of the patient (5-point scale rang- ing from very unsatisfied to very satisfied). For GPs in de intervention group the T2 questionnaire also included Results three multiple-choice questions to evaluate the case-spe- In total 481 GPs were invited to participate in this pilot cific AMSS recommendations. study, of which 75 GPs agreed to participate and 27 GPs included at least one patient (37% active GPs). Together they included 101 patients of which 66 (66.7%) com- Process evaluation pleted the AMSS questionnaire (Fig. 2). Table 1 describes At the end of the inclusion period, the GPs in the inter- the included GPs and patients. There was no significant vention group completed a questionnaire to evaluate difference in the number of (preliminary) diagnoses the usefulness of all the AMSS recommendations they reported by the GPs in the intervention versus the con- received during the study and to evaluate the utility of trol group. Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 4 of 10 GPs invited n=481 GPs GPs not responding responding n=112 n=369 GPs included GPs excluded* n=75 n=37 Randomisation GPs intervention group GPs control group n=36 n=39 GPs active GPs inactive GPs active GPs inactive n=15 (42%)^ n=21 (58%) n=12 (31%) n=27 (69%) Patients included GPs interviewed Patients included GPs interviewed by GP (T1) n=4 by GP (T1) n=6 n=58 n=42 Patients completed AMSS Patients completed AMSS questionnaire n=42 (72%) questionnaire n=24 (57%) Advice sent to GP n=42 GPs reported GPs reported diagnosis for diagnosis for patient (T2) patient (T2) n=35 (83%) n=18 (75%) Fig. 2 Flow chart of the pilot study. *GP refused to participate because of being busy/no priority (n = 17), did not expect relevant cases (n = 4), moving/changes in practice (n = 6), performs sIgE at other laboratory (n = 4), responded too late (n = 2) or other reason (n = 4). ^Percentages represent those of the previous step in the chart. In total 101 patients were included by GPs. However, for one patient it was unclear by which GP she was included and thus whether the GP was from the intervention or control group. Also, she did not complete the AMSS questionnaire and was therefore excluded from further analysis Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 5 of 10 Table 1 Descriptive characteristics of the GPs and the patient characteristics at T1 Intervention group (n = 36) Control group (n = 39) GPs Sex, n (m/f ) 25/11 28/11 Households in community, n (< 20,000/> 20,000) 23/13 27/12 Intervention group (n = 58) Control group (n = 42) Patients Sex, n (m/f ) 18/39 13/29 Age, mean in years (SD) 28.7 (18.6) 28.5 (17.9) Age, n (child/adult) 20/38 16/26 Diagnosis by GP, n (%) Allergic rhinitis 36 (62) 24 (57) Asthma 11 (19) 10 (24) Eczema 5 (9) 4 (10) Bee/wasp allergy 0 0 Medication allergy 0 2 (5) Latex allergy 0 0 Food allergy 9 (16) 8 (19) No preliminary diagnosis 3 (5) 3 (7) Other 12 (21) 6 (14) Medication prescribed by GP, n (%) 33 (57) 28 (67) Other management recommendations by GP, n (%) 29 (50) 21 (50) Referred by GP, n (%) 3 (5) 3 (7) More than one category was possible One missing Feasibility cases, whereas GPs in the control group reported this in The majority of the AMSS recommendations (93%) 72% of cases (n.s.). were sent back to the GP within 10 working days after the sIgE test results were known [mean (SD) 4.7 (4.0) Agreement between AMSS and GPs concerning diagnosis days]. At T2, significantly more agreement (AMSS +/GP +) (p = 0.016), less disagreement A (AMSS +/GP −) (p = 0.004) and a higher total agreement score (agree- Case‑specific evaluation of AMSS recommendations ment minus both disagreement A and B) (p = 0.003) con- At T2, GPs in the intervention group reported that the cerning diagnosis were found for the intervention group AMSS recommendations were complete and to-the- compared to the control group. Also, for the change of point in 80% of cases, that they largely agreed with the scores (T2 minus T1), significantly more agreement AMSS recommendations in 80% of cases and that they (p = 0.001), less disagreement A (p < 0.001) and a higher largely (71% of cases) or partly (20% of cases) followed total agreement score (p < 0.001) were found for the the AMSS recommendations. Specific patterns for not intervention than for the control group. Disagreement B (or partly) following the AMSS recommendations could did not differ significantly between the groups (Fig.  3a– not be determined. d). Table  2 shows the diagnoses reported by the GPs in the intervention group and control group at T1 and T2 and the probable diagnosis by the AMSS. GPs’ satisfaction with their own management At T2, GPs in the intervention group reported being sat- Agreement between AMSS and GPs concerning medication isfied to very satisfied regarding the diagnosis and man - Table  3 shows the medication reported by the GPs in agement recommendation for their patient in 88% of the intervention group and control group at T1 and T2 Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 6 of 10 (c) Disagreement B (diagnosis) (a) Agreement (diagnosis) 1.8 1.8 1.6 1.6 1.4 1.4 1.2 1.2 Intervention group Intervention group 0.8 0.8 Control group Control group 0.6 0.6 0.4 0.4 0.2 0.2 AMSS vs T1GAMSS vs T2G AMSS vs T1GAMSS vs T2G (d) Total agreement score (diagnosis) (b) Disagreement A (diagnosis) 0.6 1.8 0.4 1.6 0.2 1.4 AMSS vs T1GAMSS vs T2G 1.2 -0.2 Intervention group -0.4 Intervention group Control group 0.8 -0.6 Control group 0.6 -0.8 0.4 -1 0.2 -1.2 0 -1.4 AMSS vs T1GAMSS vs T2G Fig. 3 Agreement concerning diagnosis by AMSS and diagnosis reported by GPs ( T1 and T2). Selection based on complete data sets at T1 and T2 (intervention group n = 35, control group n = 18). a Agreement (GP +/AMSS +), b disagreement A (AMSS +/GP −), c disagreement B (AMSS −/ GP +), d total agreement score (agreement minus both disagreement A and B) Table 2 Diagnoses reported by  the  GPs in  intervention group and  control group at  T1 and  T2 and  the  probable diagnosis by the AMSS (more than one diagnosis possible per patient) Intervention group (n = 35) Control group (n = 18) T1 AMSS T2 T1 AMSS T2 Allergic rhinitis 20 (57) 33 (94) 22 (63) 10 (56) 17 (94) 7 (39) Asthma 9 (26) 25 (71) 14 (40) 7 (39) 15 (83) 6 (33) Eczema 4 (11) 4 (11) 5 (14) 1 (6) 4 (22) 1 (6) Bee/wasp allergy 0 2 (6) 0 0 0 0 Medication allergy 0 1 (3) 1 (3) 0 1 (6) 0 Latex allergy 0 1 (3) 0 0 0 0 Food allergy 5 (14) 8 (23) 6 (17) 3 (17) 0 2 (11) Urticaria 1 (3) 1 (3) 1 (3) 0 0 0 No diagnosis 3 (9) 0 1 (3) 0 1 (6) 3 (17) Other 8 (23) 2 (6) 7 (20) 2 (11) 5 (28) 3 (17) Presented as n (%) GPs in the control group did not receive probable diagnoses from the AMSS. The AMSS formulated these probable diagnoses for evaluative purposes only and the medication recommendations of the AMSS. No disagreement A (AMSS +/GP −) at T2 (p = 0.026) with significant differences between intervention and control less disagreement in the intervention group (data not group were found regarding agreement and disagreement shown). between AMSS and GPs concerning medication, except Disagreement A (n) agreement (n) Total agreement score (n) Disagreement B (n) Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 7 of 10 Table 3 Medication reported by  the  GPs in  intervention group and  control group at  T1 and  T2 and  the  medication recommendations of the AMSS Intervention group (n = 35) Control group (n = 18) T1 AMSS T2 T1 AMSS T2 Antihistamines Nasal 2 (6) 1 (3) 3 (9) 0 1 (6) 0 Ocular 2 (6) 0 2 (6) 1 (6) 0 1 (6) Oral 10 (29) 20 (57) 15 (43) 4 (22) 7 (39) 4 (22) Corticosteroids Nasal 9 (26) 16 (46) 15 (43) 3 (17) 9 (50) 4 (22) Pulmonary 4 (11) 5 (14) 6 (17) 2 (11) 2 (11) 1 (6) Oral 0 0 0 1 (6) 0 1 (6) Cutaneous class 1 1 (3) 2 (6) 1 (3) 0 2 (11) 0 Cutaneous class 2 1 (3) 3 (9) 1 (3) 0 3 (17) 0 Cutaneous class 3 0 0 0 1 (6) 1 (6) 1 (6) Cutaneous class 4 0 0 0 0 0 0 B‑sympathicomimetics Short‑acting 7 (20) 20 (57) 9 (26) 3 (17) 13 (72) 4 (22) Long‑acting 0 0 1 (3) 0 1 (6) 0 Leukotrien antagonists 0 0 0 1 (6) 0 1 (6) Combination therapy (corticosteroids with 0 1 (3) 1 (3) 2 (11) 0 2 (11) B‑sympathicomimetics) Decongestants 0 0 0 0 0 0 Emollients 1 (3) 7 (20) 1 (3) 1 (6) 5 (28) 1 (6) Epinephrine auto‑injector 0 8 (23) 2 (6) 0 3 (17) 0 GPs did not report considering immunotherapy for any patients. The AMSS advised immunotherapy as a follow‑up option after instituting pharmacotherapy 16 times (46%) in the intervention group and 9 times (50%) in the control group. The AMSS advised venom immunotherapy for a single patient Presented as n (%) GPs in the control group did not receive AMSS recommendations. The AMSS formulated these recommendations for evaluative purposes only For two persons the AMSS advised H2 antagonist as urticaria medication Agreement between AMSS and GPs concerning referrals led to (at least a small) improvement in care and quality At T1, GPs in the intervention and control group (Fig.  4b) and wished the AMSS to be integrated into the reported 3 (9%) and 1 (6%) referrals, respectively. The GP information system in the future (Fig. 4c). AMSS advised 9 (26%) and 5 (29%) referrals in the inter- vention and control groups, respectively. At T2 the GPs Qualitative evaluation in the intervention and control group reported 10 (29%) Saturation occurred after ten interviews with inactive and 3 (18%) referrals, respectively (p = 0.504). No sig- GPs (i.e. randomized GPs who did not include patients). nificant differences between intervention and control GPs mentioned several reasons for not including patients group were found regarding agreement and disagreement into this study: lack of time (n = 6), not appreciating the between AMSS and GPs concerning referrals (data not importance of the study (n = 5), and forgetting about shown). the study (n = 4). All GPs emphasized the importance of reminders in order to stay involved. Younger GPs pre- Process evaluation ferred an email as reminder and older GPs preferred a Of the 15 active GPs in the intervention group, 14 visit. No GP indicated that the AMSS system was antici- returned the overall evaluation questionnaire. However, pated to be ineffective, or unworkable. one questionnaire was returned blank, thus 13 question- naires were eligible for analysis. The AMSS was rated by Discussion the GPs with an average score of 6.7 out of 10. The major - The results of this pilot study suggest that the AMSS ity found the AMSS recommendations helpful in mak- is feasible in primary care. In addition, a majority of ing the diagnosis and determining the management of the GPs reported that they completely followed the patients (Fig.  4a). A majority also found that the AMSS AMSS recommendations. This was confirmed by the Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 8 of 10 to disapproval or anticipated disappointment with the (a) Was the AMSS advice helpful with ...? AMSS. This is an important finding in the light of com - puter decision support systems within routine care. At interpretation of sIgE least in asthma it has been shown that these support sys- diagnosis tems are rarely used and the advice is not followed [19]. extremely This is in contrast to our study where we demonstrated very medication that the GPs were following the AMSS advice. moderate Initially, we hypothesized that the AMSS would pre- referral a little vent referrals. However, in this study GPs in the interven- not other management tion group tend to refer patients to specialist care more not completed often than GPs in the control group. It may be that GPs in consultation the control group performing usual care underestimated 0% 20%40% 60%80% 100% the problems and severity of allergic patients, whereas (b) Did the AMSS advice result in ...? the GPs in the intervention group were alerted by AMSS recommendations which encouraged them to refer the care improvement very large patient on to specialist care. In principal, this may not be large a bad thing, as for example one would not wish to delay quality improvement moderate the referral of a patient with sIgE mediated anaphylaxis small time saving [20]. Based on these findings, the emphasis for future no 0% 20%40% 60%80% 100% work may shift from providing GPs with recommenda- tions allowing them to manage more allergy patients in (c) Future developments for AMSS ... primary care, to identifying in which environment (pri- integration in GP information mary or specialist care) the care of the allergic patient system is likely to be optimized. This suggests perhaps that the without sIgE AMSS, after further refinements may also be used as a agee advice on which sIgE tool to enable care stratification. disagree A potential strength of the AMSS in the future is the prioritising severe patients no opinion possible learning effect for GPs using this system. By electronic history not completed questionnaire receiving individualized patient-specific feedback on each case, GPs could become more effective in identifying, no future managing and referring allergic patients. This will also be 0% 20%40% 60%80% 100% expected to have a learning effect on whether sIgE deter - Fig. 4 a Helpfulness of the AMSS recommendations, b minations are required or not and how they should be improvements brought about by the AMSS, c further developments of the AMSS (as indicated by the GPs in the intervention group) interpreted. In this way, the AMSS meets the unmet need of GPs having difficulty with interpretation of sIgE test results [9, 21]. Moreover, this direct patient-related learn- ing is likely to improve care for patients with allergies in greater agreement concerning diagnoses between GPs primary care [22, 23]. In addition, the AMSS should be and AMSS in the intervention group compared to the computerized in the future and recommendations should control group (usual care). The agreement concerning preferably be accessed via the GP’s information system medication or referral between GPs and AMSS did not in a digital format [19]. Other future developments may differ between the intervention and the control group. include using the AMSS to guide and rationalize sIgE The active GPs in the intervention group were reasonably testing and prioritizing referral to secondary care based positive about the AMSS and foresaw the usefulness of on severity as ascertained by the AMSS. These develop - the AMSS in the future. ments could further improve the efficiency of the AMSS To our knowledge this is the first study that investigates and may contribute to the development of an integrated a comprehensive allergy support tool in real primary care care pathway for allergic patients [24, 25]. practices. In the past, only one partly comparable initia- One of the strengths of this study is that it was per- tive was undertaken in the allergy field [18]. However, formed in real primary care practices using a cluster that system added simple standardized sentences to sIgE randomized design. Therefore it gives robust informa - test outcomes and was not based on an extensive, struc- tion on practical issues relating to the use of the AMSS, tured clinical history. The various reasons mentioned by such as performance and feasibility. In addition, it also inactive GPs who did not enrol patients in our current provides preliminary effect measurements. Furthermore, pilot study do not suggest that non-participation was due Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 9 of 10 of Groningen, Teaching Unit, Department of Social Psychology, Groningen, the randomized pilot study was enriched with a ques- The Netherlands. University of Groningen, University Medical Center Gron‑ tionnaire-based evaluation under the active GPs in the ingen, Department of Allergology, Groningen, The Netherlands. University intervention group and a qualitative evaluation under the of Groningen, University Medical Center Groningen, Department of Dermatol‑ ogy, Groningen, The Netherlands. University of Groningen, University Medical inactive GPs, together providing a broad insight into the Center Groningen, Department of Pediatric Pulmonology and Pediatric potential utility of the AMSS in primary care. Allergy, Groningen, The Netherlands. A limitation of this study is that the AMSS question- Acknowledgements naire is not extensively validated. However, in an earlier We would like to thank the GPs who participated in this study. In addition, study we showed good agreement (69.2%) between spe- we would like to thank Jolanda Hilgen from Certe for providing the sIgE test cialist’s recommendations (gold standard) and recom- outcomes and medical master students Rixt Brouwer and Ester Klaver for their support in the logistics during the inclusion period of this study. mendations generated by the AMSS [15]. In addition, this pilot study showed that the AMSS questionnaire is Competing interests feasible to advise GPs on diagnosis and management of The authors declare that they have no competing interests. allergic patients in primary care and in that sense the Availability of data and materials questionnaire showed face validity. In addition, the gen- The datasets used and analyzed during the current study are available from eralizability of the study may be questioned because of the corresponding author on reasonable request. the relatively low number of included patients. However, Consent for publication since this was a pilot study we had neither the intention Not applicable. nor the capacity to include large numbers of patients. Ethics approval and consent to participate Larger numbers of patients are needed to further vali- This pilot study was approved by the medical ethics committee of the Univer‑ date, refine and computerize the AMSS before rolling it sity Medical Center Groningen (METc 2013/129) who deemed that the study out to full scale. Finally, it should be noted that a history did not fall within the Dutch Medical Research Involving Human Subjects Act. Participation was voluntary, all participants received written information about questionnaire such as used in the AMSS is not intended the study and all participants signed an informed consent form. to replace a specialist consultation, but rather to support GPs. GPs will remain ultimately responsible and autono- Funding This work was supported by a grant from University Medical Center Groningen mous and may always decide to deviate from the recom- (CDO12.0060/round 2012‑2/nr.140). mendations of the AMSS. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub‑ Conclusion lished maps and institutional affiliations. In conclusion, the AMSS may be considered feasible for primary care. A majority of the GPs reported that they Received: 30 November 2017 Accepted: 23 April 2018 followed the AMSS recommendations completely, that they were reasonably positive about the utility of the AMSS, and that they were optimistic about future devel- References opments of this system. However, further refinements of 1. Asher MI, Montefort S, Bjorksten B, et al. 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Abstract

Background: The allergy management support system (AMSS) was developed to assist general practitioners (GPs) to handle the increasing burden of allergic diseases and facilitates the diagnosis and management of allergy. The aim of this cluster‑ randomized controlled pilot study was to test the feasibility of this AMSS for primary care. Methods: GPs received diagnostic and management recommendations generated by the AMSS in addition to sIgE‑ test results (intervention) or GPs received sIgE‑ test results only (control). The AMSS recommendations are based on the previously developed patient‑ completed AMSS questionnaire and sIgE‑ test results. The AMSS was considered feasible when > 70% of the AMSS recommendations were sent to the GP within ten working days of sIgE‑ testing. GPs completed a questionnaire on their diagnosis and management before ( T1) and after ( T2) receiving sIgE test results. Agreement and disagreement concerning diagnosis, medication and referrals between GPs and AMSS was investi‑ gated at T1 and T2. A total agreement score between GPs and AMSS was calculated. GPs in the intervention group completed a questionnaire to evaluate the utility of the AMSS. Semi‑ structured interviews were used to explore the motivation of GPs who did not include patients in this pilot study. Results: Twenty‑ seven GPs included 101 patients. Forty‑ two patients (72%) completed the AMSS questionnaire in the intervention group. The majority of the AMSS recommendations (93%) were returned to the GP within 10 working days after sIgE‑ test results were known [mean (SD) 4.7 (4.0) working days]. GPs in the intervention group reported largely following the AMSS recommendations in 71% of cases. The total agreement scores concerning diagnosis were significantly higher (p < 0.001) in the intervention group than the control group [mean (SD); 0.9 (1.8) vs − 0.8 (1.0)]. The agreement concerning medication or referral between GPs and AMSS did not differ between the intervention and the control group. GPs in the intervention group were reasonably positive about the AMSS. Not enrolling patients was not caused by anticipated ineffectiveness of the AMSS. Conclusion: The AMSS can be considered to be feasible for primary care. GPs tend to follow the AMSS recommenda‑ tions. The AMSS may contribute to the empowerment of GPs to better manage allergy patients in primary care. Trial registration ISRCTN ISRCTN36780877. Registered 23 November 2017 (retrospectively registered) Keywords: Allergy, Diagnosis, Feasibility, Management support system, Primary care *Correspondence: b.m.j.flokstra@umcg.nl University of Groningen, University Medical Center Groningen, Department of General Practice, Internal Postcode FA21, PO Box 196, 9700 AD Groningen, The Netherlands Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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. Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 2 of 10 results only. GPs included patients in the study during Background a 6-month period (from January 2014 until July 2014). Allergy is one of the most common chronic diseases with This pilot study was approved by the local medical ethics the number of people suffering from allergic diseases committee (METc 2013/129) who deemed that the study increasing worldwide [1–4]. Currently, more than 150 did not fall within the Dutch Medical Research Involv- million people in Europe experience allergic symptoms ing Human Subjects Act. Participation was voluntary, all [5]. The number of certified allergists per head of popu - participants received written information about the study lation ranges from 1:1,240,000 to 1:16,000 in European and all participants signed an informed consent form. countries [6]. About 50% of all children under 18  years visit their general practitioner (GP) for allergic symptoms [7]. Diagnosis and management of patients suspected of Participants allergy is often performed by GPs. In many cases, espe- All GPs allied to a single regional GP laboratory in the cially where there are very few allergists operating in northern part of the Netherlands were invited to partici- large populations, GPs are exclusively responsible for pate in this pilot study. The practices of GPs that agreed providing allergy care [8]. to participate were randomized to the intervention or GPs report having difficulties in diagnosing and man - the control group. The GPs included eligible patients aging allergic patients, including the interpretation (both children and adults). The only inclusion criterion of specific IgE (sIgE), which they attribute to a lack of was that the GP had ordered a sIgE test (usually screen- allergy training [9]. Of the major allergic diseases, food ing of inhalant allergens (grass pollen, tree pollen, house allergy has been reported by GPs as the most trouble- dust mite, cat, dog, moulds, weed pollen) or food aller- some [10, 11]. In addition, it has been shown that of the gens (hen’s egg, milk, cod, wheat, peanut, soy) for that case mix of patients referred to a regional allergy service particular patient regarding an allergy related problem. by GPs, only 43% of patients were diagnosed with an IgE There were no explicit exclusion criteria. A formal power mediated allergic disease [12]. In the United Kingdom, it calculation was not applicable, since this is a pilot study has been reported that probably a quarter and maybe half which aims to investigate the feasibility of the AMSS for of allergy referrals to secondary care may be dealt with primary care. in primary care by a GP with special interest in allergy [13]. These results demonstrate that allergy management The allergy management support system (AMSS) in primary care is not optimal in most European coun- Participating patients in the intervention and control tries [14]. group completed the AMSS questionnaire and sent Since the specialist-based allergy care model will the questionnaire to the AMSS researchers for analy- become unsustainable with increasing allergy preva- sis together with the sIgE test results. Previously devel- lence, a new allergy care model with a more important oped algorithms (for adults and children) were used to role for the GP is mandatory [8]. Therefore, we devel - allocate patients to predefined diagnostic categories and oped an allergy management support system (AMSS) to consequent recommendations for management [15]. support GPs in diagnosing and managing patients with In addition, the AMSS questionnaire, sIgE test results IgE-mediated allergy in primary care [11, 15]. Based on and resultant AMSS recommendations were checked a patient-reported history questionnaire and specific IgE by allergy specialists for inaccuracies or ambiguities. An (sIgE) blood test results, we could demonstrate that the AMSS advice was formulated for patients in the interven- AMSS is able to provide a probable diagnosis and recom- tion and control group. The AMSS recommendations, mendations on management of allergic disorders for GPs together with a copy of the completed AMSS question- [15]. The primary aim of this pilot study was to test the naire and the sIgE test outcome, were sent only to the feasibility of an AMSS for primary care. In addition, pre- GPs in the intervention group by post (Fig. 1). The AMSS liminary effects of the AMSS on diagnosis, medication recommendations formulated for patients in the control and referrals were investigated. Finally, an evaluation of group were for evaluative purposes only and were not the AMSS by the GPs was carried out. made available to the GPs in the control group. Methods Measures in patients Study design Participating patients in the intervention and control Using a cluster randomized controlled design, GPs in group completed the AMSS questionnaire which consists the intervention group received AMSS recommenda- of 12 (mainly) multiple-choice questions on symptoms, tions in addition to sIgE test results, while GPs in the triggers, severity, medication and symptom control of control group performed usual care based on sIgE test their allergic condition(s) [15]. Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 3 of 10 the AMSS for primary care. This questionnaire consisted of 13 multiple-choice questions and one question to rate the AMSS system with a score between 1 (worst) and 10 (best). Qualitative evaluation After the inclusion period, it turned out that 27 (36%) of the 75 GPs included patients in the study. Qualita- tive research was undertaken to eliminate possible (self ) selection bias and ascertain the generalizability of the results. Semi-structured interviews were used to explore the motivation of GPs who did not include patients in the pilot study. In order to obtain diversity in the qualita- tive sample, GPs were purposively selected based on the allocation of the GP to the intervention or control group, sex of the GP and location of the GP’s practice. GPs were interviewed until saturation was reached. Interviews were transcribed verbatim and analyzed using Atlas.ti based on the grounded theory [16, 17]. Statistical analysis The AMSS was considered feasible if > 70% of the AMSS recommendations was sent to the GP within 10 working days of sIgE testing. Descriptive statistics included mean (SD) and percentages. Non-parametric statistics were Fig. 1 Schematic representation of the allergy management support performed using Mann–Whitney U test or Fisher exact system (AMSS) [15] test. Agreement and disagreement concerning diagnosis, medication and referrals between GPs and AMSS were investigated at T1 and T2. For each patient, agreement was the number of diagnoses made by both the AMSS Measures in GPs and the GP. There were two types of disagreement: the Efficacy measure and case‑specific evaluation first was the number of diagnoses made by the AMSS but GPs in both groups completed a short questionnaire with not by the GP (referred to hereafter as disagreement A) multiple-choice questions on diagnosis and management and the second was the number of diagnoses made by the (medication, referral and/or non-pharmacotherapeutic GP but not by the AMSS (disagreement B). A total agree- recommendations). This questionnaire was completed ment score was then calculated as agreement minus both on two occasions: at the time of inclusion of the patient disagreement A and B. Finally, the change of the scores (T1) and at the time the sIgE test outcomes (and in the were calculated as T2 scores minus T1 scores. The same case of the intervention group, the AMSS recommenda- methodology was used for (dis)agreement concerning tions) were known (T2). In addition, the T2 question- medication prescriptions and referrals. The data was ana - naire included a question on the GPs’ satisfaction with lysed using SPSS22.0 (IBM, Chicago, USA). their own management of the patient (5-point scale rang- ing from very unsatisfied to very satisfied). For GPs in de intervention group the T2 questionnaire also included Results three multiple-choice questions to evaluate the case-spe- In total 481 GPs were invited to participate in this pilot cific AMSS recommendations. study, of which 75 GPs agreed to participate and 27 GPs included at least one patient (37% active GPs). Together they included 101 patients of which 66 (66.7%) com- Process evaluation pleted the AMSS questionnaire (Fig. 2). Table 1 describes At the end of the inclusion period, the GPs in the inter- the included GPs and patients. There was no significant vention group completed a questionnaire to evaluate difference in the number of (preliminary) diagnoses the usefulness of all the AMSS recommendations they reported by the GPs in the intervention versus the con- received during the study and to evaluate the utility of trol group. Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 4 of 10 GPs invited n=481 GPs GPs not responding responding n=112 n=369 GPs included GPs excluded* n=75 n=37 Randomisation GPs intervention group GPs control group n=36 n=39 GPs active GPs inactive GPs active GPs inactive n=15 (42%)^ n=21 (58%) n=12 (31%) n=27 (69%) Patients included GPs interviewed Patients included GPs interviewed by GP (T1) n=4 by GP (T1) n=6 n=58 n=42 Patients completed AMSS Patients completed AMSS questionnaire n=42 (72%) questionnaire n=24 (57%) Advice sent to GP n=42 GPs reported GPs reported diagnosis for diagnosis for patient (T2) patient (T2) n=35 (83%) n=18 (75%) Fig. 2 Flow chart of the pilot study. *GP refused to participate because of being busy/no priority (n = 17), did not expect relevant cases (n = 4), moving/changes in practice (n = 6), performs sIgE at other laboratory (n = 4), responded too late (n = 2) or other reason (n = 4). ^Percentages represent those of the previous step in the chart. In total 101 patients were included by GPs. However, for one patient it was unclear by which GP she was included and thus whether the GP was from the intervention or control group. Also, she did not complete the AMSS questionnaire and was therefore excluded from further analysis Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 5 of 10 Table 1 Descriptive characteristics of the GPs and the patient characteristics at T1 Intervention group (n = 36) Control group (n = 39) GPs Sex, n (m/f ) 25/11 28/11 Households in community, n (< 20,000/> 20,000) 23/13 27/12 Intervention group (n = 58) Control group (n = 42) Patients Sex, n (m/f ) 18/39 13/29 Age, mean in years (SD) 28.7 (18.6) 28.5 (17.9) Age, n (child/adult) 20/38 16/26 Diagnosis by GP, n (%) Allergic rhinitis 36 (62) 24 (57) Asthma 11 (19) 10 (24) Eczema 5 (9) 4 (10) Bee/wasp allergy 0 0 Medication allergy 0 2 (5) Latex allergy 0 0 Food allergy 9 (16) 8 (19) No preliminary diagnosis 3 (5) 3 (7) Other 12 (21) 6 (14) Medication prescribed by GP, n (%) 33 (57) 28 (67) Other management recommendations by GP, n (%) 29 (50) 21 (50) Referred by GP, n (%) 3 (5) 3 (7) More than one category was possible One missing Feasibility cases, whereas GPs in the control group reported this in The majority of the AMSS recommendations (93%) 72% of cases (n.s.). were sent back to the GP within 10 working days after the sIgE test results were known [mean (SD) 4.7 (4.0) Agreement between AMSS and GPs concerning diagnosis days]. At T2, significantly more agreement (AMSS +/GP +) (p = 0.016), less disagreement A (AMSS +/GP −) (p = 0.004) and a higher total agreement score (agree- Case‑specific evaluation of AMSS recommendations ment minus both disagreement A and B) (p = 0.003) con- At T2, GPs in the intervention group reported that the cerning diagnosis were found for the intervention group AMSS recommendations were complete and to-the- compared to the control group. Also, for the change of point in 80% of cases, that they largely agreed with the scores (T2 minus T1), significantly more agreement AMSS recommendations in 80% of cases and that they (p = 0.001), less disagreement A (p < 0.001) and a higher largely (71% of cases) or partly (20% of cases) followed total agreement score (p < 0.001) were found for the the AMSS recommendations. Specific patterns for not intervention than for the control group. Disagreement B (or partly) following the AMSS recommendations could did not differ significantly between the groups (Fig.  3a– not be determined. d). Table  2 shows the diagnoses reported by the GPs in the intervention group and control group at T1 and T2 and the probable diagnosis by the AMSS. GPs’ satisfaction with their own management At T2, GPs in the intervention group reported being sat- Agreement between AMSS and GPs concerning medication isfied to very satisfied regarding the diagnosis and man - Table  3 shows the medication reported by the GPs in agement recommendation for their patient in 88% of the intervention group and control group at T1 and T2 Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 6 of 10 (c) Disagreement B (diagnosis) (a) Agreement (diagnosis) 1.8 1.8 1.6 1.6 1.4 1.4 1.2 1.2 Intervention group Intervention group 0.8 0.8 Control group Control group 0.6 0.6 0.4 0.4 0.2 0.2 AMSS vs T1GAMSS vs T2G AMSS vs T1GAMSS vs T2G (d) Total agreement score (diagnosis) (b) Disagreement A (diagnosis) 0.6 1.8 0.4 1.6 0.2 1.4 AMSS vs T1GAMSS vs T2G 1.2 -0.2 Intervention group -0.4 Intervention group Control group 0.8 -0.6 Control group 0.6 -0.8 0.4 -1 0.2 -1.2 0 -1.4 AMSS vs T1GAMSS vs T2G Fig. 3 Agreement concerning diagnosis by AMSS and diagnosis reported by GPs ( T1 and T2). Selection based on complete data sets at T1 and T2 (intervention group n = 35, control group n = 18). a Agreement (GP +/AMSS +), b disagreement A (AMSS +/GP −), c disagreement B (AMSS −/ GP +), d total agreement score (agreement minus both disagreement A and B) Table 2 Diagnoses reported by  the  GPs in  intervention group and  control group at  T1 and  T2 and  the  probable diagnosis by the AMSS (more than one diagnosis possible per patient) Intervention group (n = 35) Control group (n = 18) T1 AMSS T2 T1 AMSS T2 Allergic rhinitis 20 (57) 33 (94) 22 (63) 10 (56) 17 (94) 7 (39) Asthma 9 (26) 25 (71) 14 (40) 7 (39) 15 (83) 6 (33) Eczema 4 (11) 4 (11) 5 (14) 1 (6) 4 (22) 1 (6) Bee/wasp allergy 0 2 (6) 0 0 0 0 Medication allergy 0 1 (3) 1 (3) 0 1 (6) 0 Latex allergy 0 1 (3) 0 0 0 0 Food allergy 5 (14) 8 (23) 6 (17) 3 (17) 0 2 (11) Urticaria 1 (3) 1 (3) 1 (3) 0 0 0 No diagnosis 3 (9) 0 1 (3) 0 1 (6) 3 (17) Other 8 (23) 2 (6) 7 (20) 2 (11) 5 (28) 3 (17) Presented as n (%) GPs in the control group did not receive probable diagnoses from the AMSS. The AMSS formulated these probable diagnoses for evaluative purposes only and the medication recommendations of the AMSS. No disagreement A (AMSS +/GP −) at T2 (p = 0.026) with significant differences between intervention and control less disagreement in the intervention group (data not group were found regarding agreement and disagreement shown). between AMSS and GPs concerning medication, except Disagreement A (n) agreement (n) Total agreement score (n) Disagreement B (n) Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 7 of 10 Table 3 Medication reported by  the  GPs in  intervention group and  control group at  T1 and  T2 and  the  medication recommendations of the AMSS Intervention group (n = 35) Control group (n = 18) T1 AMSS T2 T1 AMSS T2 Antihistamines Nasal 2 (6) 1 (3) 3 (9) 0 1 (6) 0 Ocular 2 (6) 0 2 (6) 1 (6) 0 1 (6) Oral 10 (29) 20 (57) 15 (43) 4 (22) 7 (39) 4 (22) Corticosteroids Nasal 9 (26) 16 (46) 15 (43) 3 (17) 9 (50) 4 (22) Pulmonary 4 (11) 5 (14) 6 (17) 2 (11) 2 (11) 1 (6) Oral 0 0 0 1 (6) 0 1 (6) Cutaneous class 1 1 (3) 2 (6) 1 (3) 0 2 (11) 0 Cutaneous class 2 1 (3) 3 (9) 1 (3) 0 3 (17) 0 Cutaneous class 3 0 0 0 1 (6) 1 (6) 1 (6) Cutaneous class 4 0 0 0 0 0 0 B‑sympathicomimetics Short‑acting 7 (20) 20 (57) 9 (26) 3 (17) 13 (72) 4 (22) Long‑acting 0 0 1 (3) 0 1 (6) 0 Leukotrien antagonists 0 0 0 1 (6) 0 1 (6) Combination therapy (corticosteroids with 0 1 (3) 1 (3) 2 (11) 0 2 (11) B‑sympathicomimetics) Decongestants 0 0 0 0 0 0 Emollients 1 (3) 7 (20) 1 (3) 1 (6) 5 (28) 1 (6) Epinephrine auto‑injector 0 8 (23) 2 (6) 0 3 (17) 0 GPs did not report considering immunotherapy for any patients. The AMSS advised immunotherapy as a follow‑up option after instituting pharmacotherapy 16 times (46%) in the intervention group and 9 times (50%) in the control group. The AMSS advised venom immunotherapy for a single patient Presented as n (%) GPs in the control group did not receive AMSS recommendations. The AMSS formulated these recommendations for evaluative purposes only For two persons the AMSS advised H2 antagonist as urticaria medication Agreement between AMSS and GPs concerning referrals led to (at least a small) improvement in care and quality At T1, GPs in the intervention and control group (Fig.  4b) and wished the AMSS to be integrated into the reported 3 (9%) and 1 (6%) referrals, respectively. The GP information system in the future (Fig. 4c). AMSS advised 9 (26%) and 5 (29%) referrals in the inter- vention and control groups, respectively. At T2 the GPs Qualitative evaluation in the intervention and control group reported 10 (29%) Saturation occurred after ten interviews with inactive and 3 (18%) referrals, respectively (p = 0.504). No sig- GPs (i.e. randomized GPs who did not include patients). nificant differences between intervention and control GPs mentioned several reasons for not including patients group were found regarding agreement and disagreement into this study: lack of time (n = 6), not appreciating the between AMSS and GPs concerning referrals (data not importance of the study (n = 5), and forgetting about shown). the study (n = 4). All GPs emphasized the importance of reminders in order to stay involved. Younger GPs pre- Process evaluation ferred an email as reminder and older GPs preferred a Of the 15 active GPs in the intervention group, 14 visit. No GP indicated that the AMSS system was antici- returned the overall evaluation questionnaire. However, pated to be ineffective, or unworkable. one questionnaire was returned blank, thus 13 question- naires were eligible for analysis. The AMSS was rated by Discussion the GPs with an average score of 6.7 out of 10. The major - The results of this pilot study suggest that the AMSS ity found the AMSS recommendations helpful in mak- is feasible in primary care. In addition, a majority of ing the diagnosis and determining the management of the GPs reported that they completely followed the patients (Fig.  4a). A majority also found that the AMSS AMSS recommendations. This was confirmed by the Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 8 of 10 to disapproval or anticipated disappointment with the (a) Was the AMSS advice helpful with ...? AMSS. This is an important finding in the light of com - puter decision support systems within routine care. At interpretation of sIgE least in asthma it has been shown that these support sys- diagnosis tems are rarely used and the advice is not followed [19]. extremely This is in contrast to our study where we demonstrated very medication that the GPs were following the AMSS advice. moderate Initially, we hypothesized that the AMSS would pre- referral a little vent referrals. However, in this study GPs in the interven- not other management tion group tend to refer patients to specialist care more not completed often than GPs in the control group. It may be that GPs in consultation the control group performing usual care underestimated 0% 20%40% 60%80% 100% the problems and severity of allergic patients, whereas (b) Did the AMSS advice result in ...? the GPs in the intervention group were alerted by AMSS recommendations which encouraged them to refer the care improvement very large patient on to specialist care. In principal, this may not be large a bad thing, as for example one would not wish to delay quality improvement moderate the referral of a patient with sIgE mediated anaphylaxis small time saving [20]. Based on these findings, the emphasis for future no 0% 20%40% 60%80% 100% work may shift from providing GPs with recommenda- tions allowing them to manage more allergy patients in (c) Future developments for AMSS ... primary care, to identifying in which environment (pri- integration in GP information mary or specialist care) the care of the allergic patient system is likely to be optimized. This suggests perhaps that the without sIgE AMSS, after further refinements may also be used as a agee advice on which sIgE tool to enable care stratification. disagree A potential strength of the AMSS in the future is the prioritising severe patients no opinion possible learning effect for GPs using this system. By electronic history not completed questionnaire receiving individualized patient-specific feedback on each case, GPs could become more effective in identifying, no future managing and referring allergic patients. This will also be 0% 20%40% 60%80% 100% expected to have a learning effect on whether sIgE deter - Fig. 4 a Helpfulness of the AMSS recommendations, b minations are required or not and how they should be improvements brought about by the AMSS, c further developments of the AMSS (as indicated by the GPs in the intervention group) interpreted. In this way, the AMSS meets the unmet need of GPs having difficulty with interpretation of sIgE test results [9, 21]. Moreover, this direct patient-related learn- ing is likely to improve care for patients with allergies in greater agreement concerning diagnoses between GPs primary care [22, 23]. In addition, the AMSS should be and AMSS in the intervention group compared to the computerized in the future and recommendations should control group (usual care). The agreement concerning preferably be accessed via the GP’s information system medication or referral between GPs and AMSS did not in a digital format [19]. Other future developments may differ between the intervention and the control group. include using the AMSS to guide and rationalize sIgE The active GPs in the intervention group were reasonably testing and prioritizing referral to secondary care based positive about the AMSS and foresaw the usefulness of on severity as ascertained by the AMSS. These develop - the AMSS in the future. ments could further improve the efficiency of the AMSS To our knowledge this is the first study that investigates and may contribute to the development of an integrated a comprehensive allergy support tool in real primary care care pathway for allergic patients [24, 25]. practices. In the past, only one partly comparable initia- One of the strengths of this study is that it was per- tive was undertaken in the allergy field [18]. However, formed in real primary care practices using a cluster that system added simple standardized sentences to sIgE randomized design. Therefore it gives robust informa - test outcomes and was not based on an extensive, struc- tion on practical issues relating to the use of the AMSS, tured clinical history. The various reasons mentioned by such as performance and feasibility. In addition, it also inactive GPs who did not enrol patients in our current provides preliminary effect measurements. Furthermore, pilot study do not suggest that non-participation was due Flokstra‑de Blok et al. Clin Transl Allergy (2018) 8:18 Page 9 of 10 of Groningen, Teaching Unit, Department of Social Psychology, Groningen, the randomized pilot study was enriched with a ques- The Netherlands. University of Groningen, University Medical Center Gron‑ tionnaire-based evaluation under the active GPs in the ingen, Department of Allergology, Groningen, The Netherlands. University intervention group and a qualitative evaluation under the of Groningen, University Medical Center Groningen, Department of Dermatol‑ ogy, Groningen, The Netherlands. University of Groningen, University Medical inactive GPs, together providing a broad insight into the Center Groningen, Department of Pediatric Pulmonology and Pediatric potential utility of the AMSS in primary care. Allergy, Groningen, The Netherlands. A limitation of this study is that the AMSS question- Acknowledgements naire is not extensively validated. However, in an earlier We would like to thank the GPs who participated in this study. In addition, study we showed good agreement (69.2%) between spe- we would like to thank Jolanda Hilgen from Certe for providing the sIgE test cialist’s recommendations (gold standard) and recom- outcomes and medical master students Rixt Brouwer and Ester Klaver for their support in the logistics during the inclusion period of this study. mendations generated by the AMSS [15]. In addition, this pilot study showed that the AMSS questionnaire is Competing interests feasible to advise GPs on diagnosis and management of The authors declare that they have no competing interests. allergic patients in primary care and in that sense the Availability of data and materials questionnaire showed face validity. In addition, the gen- The datasets used and analyzed during the current study are available from eralizability of the study may be questioned because of the corresponding author on reasonable request. the relatively low number of included patients. However, Consent for publication since this was a pilot study we had neither the intention Not applicable. nor the capacity to include large numbers of patients. Ethics approval and consent to participate Larger numbers of patients are needed to further vali- This pilot study was approved by the medical ethics committee of the Univer‑ date, refine and computerize the AMSS before rolling it sity Medical Center Groningen (METc 2013/129) who deemed that the study out to full scale. Finally, it should be noted that a history did not fall within the Dutch Medical Research Involving Human Subjects Act. Participation was voluntary, all participants received written information about questionnaire such as used in the AMSS is not intended the study and all participants signed an informed consent form. to replace a specialist consultation, but rather to support GPs. GPs will remain ultimately responsible and autono- Funding This work was supported by a grant from University Medical Center Groningen mous and may always decide to deviate from the recom- (CDO12.0060/round 2012‑2/nr.140). mendations of the AMSS. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in pub‑ Conclusion lished maps and institutional affiliations. In conclusion, the AMSS may be considered feasible for primary care. A majority of the GPs reported that they Received: 30 November 2017 Accepted: 23 April 2018 followed the AMSS recommendations completely, that they were reasonably positive about the utility of the AMSS, and that they were optimistic about future devel- References opments of this system. However, further refinements of 1. Asher MI, Montefort S, Bjorksten B, et al. 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Clinical and Translational AllergySpringer Journals

Published: May 29, 2018

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