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\begin{document}

\title{Caregiver views on virtual management of food allergy: a mixed-methods
study}



\author[1]{Edmond Chan}%
\author[2]{Samira Jeimy}%
\author[3]{Mariam Hanna}%
\author[4]{Victoria Cook}%
\author[3]{Douglas Mack}%
\author[5]{Elissa Abrams}%
\author[1]{Lianne Soller}%
\author[1]{Tiffany Wong}%
\author[5]{Jennifer Protudjer}%
\affil[1]{BC Children's Hospital}%
\affil[2]{Western University Schulich School of Medicine and Dentistry}%
\affil[3]{McMaster University}%
\affil[4]{The University of British Columbia Faculty of Medicine}%
\affil[5]{University of Manitoba}%


\vspace{-1em}



  
  \date{May 18, 2024}


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\textbf{1 Conflicts of interest}

ESC has received research support from DBV Technologies; has been a
member of advisory boards for Pfizer, Pediapharm, Leo Pharma, Kaleo,
DBV, AllerGenis, Sanofi Genzyme, Bausch Health, Avir Pharma; is a member
of the healthcare advisory board for Food Allergy Canada; was an expert
panel and coordinating committee member of the National Institute of
Allergy and Infectious Diseases (NIAID)-sponsored Guidelines for Peanut
Allergy Prevention; and was co-lead of the CSACI oral immunotherapy
guidelines.

SJ has been on speaker's bureaus for Aralez, Novartis, Astra Zeneca, and
Sanofi, and on the advisory board for Sanofi.

MH has provided speaker services for Pfizer, Pediapharm, and has been
part of an advisory board for ALK and provides privately funded OIT.

VC has been a participant on advisory boards for Sanofi Genzyme, Bausch
Health, and ALK, speaker services for Aralez Pharmaceuticals and CSL
Behring.

DM has provided consultation and speaker services for Pfizer, Aimmune,
Kaleo, Merck, Covis and Pediapharm, and has been part of an advisory
board for Pfizer and Bausch Health. He sits on the editorial board for
the Journal of Food Allergy.

EA Section Head of Anaphylaxis/Food Allergy for the Canadian Society of
Allergy and Clinical Immunology; sits on steering committee for Canada's
National Food Allergy Action Plan; moderator/speaker fees from Novartis,
GSK, Sanofi, AstraZeneca.

LS None

TW speaking engagements for Pfizer and Stallergenes Greer, Advisory
Board member for ALK and Leo Pharma

JP is the Section Head of Allied Health for the Canadian Society of
Allergy and Clinical Immunology; and sits on the steering committee for
Canada's National Food Allergy Action Plan

\textbf{2 Financial support}

Funding for this study was generously provided by J Protudjer's Start Up
Funds from the Department of Pediatrics and Child Health, University of
Manitoba; and, the Children's Hospital Research Institute of Child
Health.

\textbf{3 Keywords}

Allergy; COVID-19; hybrid care; mixed-methods; virtual care

Abstract not required per the instruction for authors.

\textbf{4 Main text starts on next page}

To the Editor:

During the first months of the COVID-19 pandemic, healthcare acutely
switched almost exclusively to virtual delivery (1, 2), with little
precedent, and even less knowledge about caregivers' comfort with such
delivery. It is unlikely that we will ever return to exclusively
in-person care (3, 4). Thus, there is a critical, but currently
unstudied, need to understand caregivers' attitudes toward virtual food
allergy management. To address this knowledge gap, we performed a
mixed-methods study in which we sought to examine caregivers' views on
virtual food allergy care.

In this embedded mixed-methods study (5), quantitative and qualitative
data were concurrently collected from English-speaking caregivers of
children \textless{}18 years being followed by an allergist for food
allergy in Canada. Between October-December 2020, caregivers were
contacted via email distribution lists from regional and national
patient organizations; and through social media.

Basic demographics and caregiver experiences with virtual care (see
Table E1 for definitions) were queried and collected in SurveyMonkey\selectlanguage{ngerman}®.
Data were described (n/N, \%, mean (standard deviation {[}SD{]}) and
compared (chi2, t-tests), using Stata® 15.1 (College Station, TX), with
p\textless{}0.05. Open-ended responses were analyzed thematically (6).
Quantitative and qualitative findings were mixed in the interpretation.
This study was approved by the University of Manitoba Health Research
Ethics Board (HS24207(H2020:384)).

Overall, 66 caregivers completed the survey, which represents 85.7\%
(66/77) who started the survey. Approximately half of caregivers had
graduate/professional degrees (30/64; 46.9\%). Half of children were age
\selectlanguage{english}[?]5 years (33/65; 50.8\%) with slightly more boys than girls included
(59.1\% vs. 40.9\%; Table 1). The three most frequently reported food
allergies were peanut (42/66; 63.6\%), tree nuts (30/66; 45.5\%) and egg
(29/66; 43.9\%). Nearly all families lived within 50 km of their
allergist.

The most frequently reported type of allergy-related care was routine
follow-up (50/66; 75.8\%; Table 2). Overall caregiver-reported
satisfaction (virtual + in-person combined) was comparable between
routine follow-up and initial assessments, oral food challenges (OFC)
and oral immunotherapy (OIT). A corresponding comparison to early food
introduction was not performed due to a low number of these visits
reported (3/66; 4.5\%). Satisfaction with virtual versus in-person care
was comparable. For example, mean satisfaction scores for initial
assessments for virtual and in-person care were 66.5+-8.0 and 81.1+-5.3,
respectively (p=0.21).

Qualitatively, caregivers described virtual allergy-related care as
having ``the benefit without the burdens'' (Figure 1). This theme
reflects caregivers' descriptions of being able to access care for their
child's allergy, without concerns for childcare for other children in
the family; losing several hours for travel and wait times; or, about
being exposed to the COVID-19 virus. As one caregiver described, virtual
allergy care could be done ``\emph{from home or work, {[}with{]} no
childcare issues, no commute time, no exposure to covid (sic)} .''
Another caregiver noted additional benefits including ``\emph{saving
money (parking and lunch fees at hospital), don't need to pull kids from
school for appointment, home setting is comfortable {[}so{]} child not
nervous.} ''

Caregivers also perceived disadvantages. The single word theme,
``Isolation,'' captures the isolation felt by parents of children with
food allergy. As a caregiver, whose child's in-person appointment for
routine allergy-testing had been moved to virtual care, commented that
virtual care contributed to feelings of isolation

\emph{{[}We are{]} feeling even more isolated as an allergy family. We
already feel we live on the periphery of society as we watch our son's
friends have birthday parties while he sits far away from everyone to
ensure his safety.}

Isolation was also described by parents of children requiring diagnostic
testing, those who were newly diagnosed, and those who were receiving
OIT. Similarly, caregivers noted the amplification of social isolation
that existed prior to the pandemic. A small minority reported ``\emph{no
advantages} '' to virtual allergy care, noting that there are
``\emph{just disadvantage(s) `cause no skin testing was
available.''}This lack of access to testing exacerbated the perception
of isolation. Likewise, isolation was described by caregivers whose
children were receiving higher risk treatment. Caregivers expressed
concern that there was no medical professional physically present to
assist if their child were to have a reaction subsequent to testing. As
noted by parents whose child had received virtual OIT expressed that, if
the child were to react, ``\emph{I am the only one here to help him} .''
Another caregiver, whose child's in-person appointment for routine
allergy-testing had been moved to virtual care, commented that virtual
care for food allergy further contributed to feelings of isolation:

In this first mixed-methods study of caregivers' experiences with food
allergy care during the COVID-19 pandemic, there were no significant
differences in caregiver satisfaction by type of care, or by type of
delivery, based on quantitative data. Qualitatively, caregivers detailed
benefits and limitations of virtual care, including amplified social
isolation.

In keeping with the theme of isolation identified herein, we identified
a similar theme in a qualitative exploration performed prior to the
COVID-19 pandemic (7). In the previous study, parents reported
``\emph{anxiety and isolation} '' and existed tenuously with allergy,
which had become their normal (7). Importantly, caregivers described
that this isolation was further exacerbated when they lacked support
from extended family and/or close friends. In the present study,
caregivers similarly described isolation, but did not speak to support
from family or friends. This may be partly attributable to the wider
isolation as a result of COVID-19-related physical distancing measures,
well beyond that experienced in virtual care. But, taken collectively,
these findings point toward a likely gap in support structures during
the pandemic, which must be addressed or otherwise places caregivers and
their children at further risk of isolation, including downstream
effects thereof.

Our mixed-methods study provided insights into specific disadvantages
that could not be captured through a quantitative survey. The COVID-19
pandemic has propelled virtual healthcare forward in ways that would
have otherwise taken generations. This type of healthcare delivery may
be a practical option even after the pandemic, particularly in rural and
remote regions, providing that there is reliable telephone and/or
internet access. We acknowledge that participants in the current study
were economically advantaged. Additional work exploring the satisfaction
of, and access to virtual care amongst economically-disadvantaged
caregivers is warranted. Shared decision making is an increasingly
important paradigm in allergy, and one which mandates a strong
physician-patient relationship (8). The findings presented herein
reinforce the need for caregivers to have a voice, particularly those in
lower socioeconomic groups, to promote high quality care. This cannot be
overstated if virtual care is to be successfully continued
post-COVID-19.

Whereas access to testing that requires in-person contact is
logistically challenging during a virtual appointment, we suggest that
this may be amendable to a hybrid model. Systems navigation is a
documented way of reducing the fragmentation and gaps in care, tailored
to address the needs and characteristics of a given patient population
(9). In an allergy context, this model may involve testing patients in
rural and remote regions with regional/local healthcare partners, after
which the results are sent to the allergist for interpretation. Future
research is warranted to explore this potential, and the related
cost-effectiveness.

In conclusion, caregivers were satisfied, yet felt socially isolated, as
a result of virtual care and more generally, food allergy. This study
provides the necessary first steps in guiding the sustainability efforts
of allergy care in this new virtual medicine era.

\emph{Edmond S. Chan MD FRCPC}

Division of Allergy and Immunology, Department of Pediatrics, The
University of British Columbia, Vancouver, BC, Canada

\emph{Samira Jeimy MD PhD FRCPC}

Division of Clinical Immunology and Allergy, Department of Medicine,
Western University, London, ON, Canada

\emph{Mariam Hanna MD FRCPC}

Department of Pediatrics, McMaster University, Hamilton, ON, Canada

\emph{Victoria E Cook MD MSc FRCPC}

Division of Allergy and Immunology, Department of Pediatrics, The
University of British Columbia, Vancouver, BC, Canada

\emph{Douglas P Mack MD FRCPC}

Department of Pediatrics, McMaster University, Hamilton, ON, Canada

\emph{Elissa M Abrams MD FRCPC}

Division of Allergy and Immunology, Department of Pediatrics, The
University of British Columbia, Vancouver, BC, Canada

Department of Pediatrics and Child Health, University of Manitoba,
Winnipeg, MB

Children's Hospital Research Institute of Manitoba, Winnipeg, MB, Canada

\emph{Lianne Soller PhD}

Division of Allergy and Immunology, Department of Pediatrics, The
University of British Columbia, Vancouver, BC, Canada

\emph{Tiffany Wong MD FRCPC}

Division of Allergy and Immunology, Department of Pediatrics, The
University of British Columbia, Vancouver, BC, Canada

\emph{Jennifer LP Protudjer PhD}

Department of Pediatrics and Child Health, University of Manitoba,
Winnipeg, MB

Children's Hospital Research Institute of Manitoba, Winnipeg, MB, Canada

Centre for Allergy Research, Karolinska Institutet, Stockholm, Sweden



\textbf{6 References}

1. Searing DA, Dutmer CM, Fleischer DM, Shaker MS, Oppenheimer J,
Grayson M, et al. A phased approach to resuming suspended
allergy/immunology clinical services. JACI: IP.
2020;S2213-98(20):30486-4.

2. Portnoy J, Waller M, Elliott T. Telemedicine in the era of COVID-19.
J Allergy Clin Immunol: In Pract. 2020;8(5):1489-91.

3. Wittmeier KDM, Protudjer JLP, Wicklow BA. Reflections on virtual care
for chronic conditions during the COVID-19 pandemic. Can J Diabetes.
2021.

4. Mack DP, Chan ES, Shaker M, Abrams EM, Wang J, Fleischer DM, et al.
Novel approaches to food management during COVID-19 inspire long-term
change. J Allergy Clin Immunol Pract. 2020;8(9):2851-7.

5. Creswell JW, Plano Clark VL. Designing and conducting mixed methods
research. Thousand Oaks, CA: Sage Publications; 2007.

6. Patton MQ. Qualitative research and evaluation methods. 3rd ed. ed.
Thousand Oaks, CA: Sage Publications; 2002.

7. Abrams EM, Simons E, Roos L, Hurst K, Protudjer JLP. Qualitative
analysis of perceived impacts on childhood food allergy on caregiver
mental health and lifestyle. Ann Allergy Asthma Immunol.
2020;S1081-1206(20):20113-7.

8. Abrams EM, Shaker M, Oppenheimer J, Davis RS, Bukstein DA, Greenhawt
M. The challenges and opportunities for shared decision making
highlighted by COVID-19. J AllErgy Clin Immunol Pract.
2020;8(8):2472-80.

9. Carter N, Valaitis RK, Lam A, Feather J, Nicholl J, Cleghorn L.
Navigation delivery models and role so navigators in primary care: a
scoping literature review. BMC Health Serv Res. 2018;18(96).

\textbf{Table E1.} List of terms and definitions\selectlanguage{english}
\begin{longtable}[]{@{}ll@{}}
\toprule
\textbf{Term} & \textbf{Definition}\tabularnewline
\midrule
\endhead
Types of food allergy-related care & Initial assessment (initial
assessment or consultation), routine follow-up appointments, early
introduction of food (feeding the infant, between about age 4-6 months,
a small amount of food to which the caregiver is concerned the infant
may be allergic), OFC and OIT.\tabularnewline
Hybrid delivery of care & A combination of both virtual and in-person
practice, without consideration of the proportion allocated per type of
delivery.\tabularnewline
Levels of parent satisfaction & Queried on a scale of 0-100,
representing lowest to highest possible satisfaction,
respectively.\tabularnewline
Virtual care & Allergy care received over the phone and/or internet, not
in-person\tabularnewline
\bottomrule
\end{longtable}

Abbreviations: \emph{OFC} Oral food challenge; \emph{OIT oral
immunotherapy}\selectlanguage{english}
\begin{longtable}[]{@{}lll@{}}
\toprule
\textbf{Table 1}. Participating family demographics (N=66) &
&\tabularnewline
\midrule
\endhead
Variable & n & \%\tabularnewline
Child's age group (years) & &\tabularnewline
1-2 & 15 & 23.1\tabularnewline
3-5 & 18 & 27.7\tabularnewline
6-10 & 21 & 32.3\tabularnewline
11-18 & 11 & 16.9\tabularnewline
Child's Gender & &\tabularnewline
Boys & 39 & 59.1\tabularnewline
Girls & 27 & 40.9\tabularnewline
Parental highest level of education (N=64) & &\tabularnewline
High school, college, trade school or undergraduate & 34 &
53.1\tabularnewline
Graduate school or professional degree & 30 & 46.9\tabularnewline
Pre-pandemic income (N=59) & &\tabularnewline
\textless{} \$100,000 & 16 & 27.1\tabularnewline
\$101,000 -\$200,000 & 29 & 49.2\tabularnewline
\textgreater{} \$201,000 & 14 & 23.7\tabularnewline
Pandemic income (N=58) & &\tabularnewline
\textless{} \$100,000 & 18 & 31.1\tabularnewline
\$101,000 -\$200,000 & 26 & 44.8\tabularnewline
\textgreater{} \$201,000 & 14 & 24.1\tabularnewline
\textbf{Allergy characteristics} & &\tabularnewline
Child's food allergies* & &\tabularnewline
Peanut & 42 & 63.6\tabularnewline
Tree nuts & 30 & 45.5\tabularnewline
Sesame & 14 & 21.2\tabularnewline
Milk & 24 & 36.4\tabularnewline
Egg & 29 & 43.9\tabularnewline
Fish & 6 & 9.1\tabularnewline
Crustaceans and molluscs & 6 & 9.1\tabularnewline
Soy & 4 & 6.1\tabularnewline
Wheat & 4 & 6.1\tabularnewline
Mustard & 2 & 3.0\tabularnewline
Legumes other than soy & 7 & 10.7\tabularnewline
Seeds other than sesame or mustard & 1 & 1.5\tabularnewline
Other & 11 & 16.7\tabularnewline
Age at diagnosis & &\tabularnewline
\textless{}12 months & 42 & 63.6\tabularnewline
1-2 years & 15 & 22.7\tabularnewline
3+ years & 9 & 13.7\tabularnewline
Do not see allergist in own province & 2 & 3.2\tabularnewline
Distance travelled to visit allergist & &\tabularnewline
\textless{} 20km & 37 & 56.1\tabularnewline
21-50km & 18 & 27.3\tabularnewline
51-100 km & 6 & 9.1\tabularnewline
100-250km & 5 & 7.5\tabularnewline
Not mutually exclusive & &\tabularnewline
\bottomrule
\end{longtable}

\textbf{Table 2.} Participating caregivers' (N=66) access to
allergy-related care, including type of delivery, during the COVID-19
pandemic\selectlanguage{english}
\begin{longtable}[]{@{}lllll@{}}
\toprule
Type of care & & & Satisfaction & Satisfaction\tabularnewline
& n & \% & mean & SD\tabularnewline
\textbf{A. Allergy-related care*} & & & &\tabularnewline
Initial assessment & 22 & 33.3 & 72.5 & 24.4\tabularnewline
Follow-up & 50 & 75.8 & 78.0 & 27.2\tabularnewline
Early introduction & 3 & 4.5 & 89.3 & 9.5\tabularnewline
Oral food challenge & 18 & 27.3 & 77.9 & 27.3\tabularnewline
Oral immunotherapy & 14 & 21.2 & 87.4 & 26.4\tabularnewline
\textbf{B. Allergy-related care by type of delivery} & \textbf{B.
Allergy-related care by type of delivery} & \textbf{B. Allergy-related
care by type of delivery} & &\tabularnewline
Initial assessment & & & &\tabularnewline
Virtual & 12 & 54.5 & 66.5 & 27.6\tabularnewline
In-person & 7 & 31.9 & 81.1 & 14.2\tabularnewline
Both & 3 & 13.6 & 76.3 & 30.7\tabularnewline
Follow-up & & & &\tabularnewline
Virtual & 35 & 70.0 & 75.2 & 29.6\tabularnewline
In-person & 14 & 28.0 & 83.6 & 20.3\tabularnewline
Both & 1 & 2.0 & 97.0 & -\tabularnewline
Early introduction & & & &\tabularnewline
Virtual & 3 & 100.0 & 89.3 & 9.5\tabularnewline
In-person & 0 & 0.0 & - & -\tabularnewline
Both & 0 & 0.0 & - & -\tabularnewline
Oral food challenge & & & &\tabularnewline
Virtual & 16 & 88.9 & 76.0 & 28.5\tabularnewline
In-person & 0 & 0.0 & - &\tabularnewline
Both & 2 & 11.1 & 93.0 & 1.4\tabularnewline
Oral immunotherapy & & & &\tabularnewline
Virtual & 8 & 57.1 & 91.5 & 9.8\tabularnewline
In-person & 0 & 0.0 & 0.0 & 0.0\tabularnewline
Both & 6 & 42.9 & 82.0 & 40.2\tabularnewline
Not mutually exclusive & & & &\tabularnewline
Abbreviation: \emph{SD} Standard deviation & Abbreviation: \emph{SD}
Standard deviation & Abbreviation: \emph{SD} Standard deviation &
&\tabularnewline
\bottomrule
\end{longtable}



\textbf{9 Figure Legend}

\textbf{Figure 1.} Qualitative perceptions of virtual allergy care

\selectlanguage{english}
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