- Email: [email protected]
Relationship between maternal and child behaviors in pediatric food allergy—an exploratory study
Letters / Ann Allergy Asthma Immunol 116 (2016) 72e88
Isotype controls had been used during the validation of basophil activation test. Statistical analyses were performed with GraphPad Prism 6.0 (GraphPad, San Diego, California). Doseeresponse curves were fitted to a 4-parameter nonlinear regression model. Data are presented as mean SEM of 14 subjects. Two-tailed t test for paired samples was used to test for differences between CD63þ cells and CD63 mean fluorescence intensity, respectively, at 4 PM and 4 AM. The significance level was set at P < .05. In this pilot study, we found that basophil sensitivity of volunteers without allergy showed diurnal changes in response to IgEdependent activation. Figure 1 shows a significant decrease in basophil sensitivity at 4 AM (n ¼ 14, P ¼ .0298) when assessed by the mean fluorescence intensity of CD63þ basophils, suggesting that basophils of persons without allergy are less sensitive early in the morning. Notably, we did not find diurnal variation of reactivity assessed by the more commonly used percentage of CD63þ cells in response to anti-IgE at 4 AM and 4 PM (P ¼ .607, data not shown). Hence, our data support the finding that the mean fluorescence intensity is an important parameter in basophil activation test. Mast cells and eosinophils, main effector cells of allergic reactions aside from basophils, recently have been found to exhibit a functional clock mechanism. Clock genes are responsible for generating the circadian rhythm and the clock has been found to control activation of mast cells and eosinophils, resulting in circadian production and release of their mediators.6 These findings assume that the circadian clock influences and controls allergic reactions and not vice versa. Moreover, blood basophil numbers display circadian variations.8 In addition, we found that the intensity of the activation marker CD63 expressed on basophils exhibits diurnal variation. Very recently, daily variations in basophil reactivity have been reported in patients with seasonal allergic rhinitis, with an increase in CD203cþ basophils at 7 AM compared with 7 PM.9 However, we analyzed the circadian rhythm of the sensitivity of basophils of volunteers without allergy. Because donor selection, time points, activation markers, and readout differed between the previous and present studies, the results are not directly comparable. Certainly, further experiments and measurements of more than 2 time points will be necessary to clarify this issue and to explain the higher frequency of allergic symptoms between midnight and morning. At activation, expression of CD63 correlates with degranulation and the release of histamine and with the severity of allergic reactions.2,10 Thus, basophil activation, mediator release, and clock gene expression around the clock and the correlation of circadian allergic symptoms of patients should be analyzed in a follow-up study. In conclusion, this pilot study provides a first hint that the circadian clock might regulate the intensity of basophil response in IgE-dependent allergic reactions. Anja Baumann, PhD* Tina Skjold, MD, PhDy Hans Jürgen Hoffmann, PhDy Axel Lorentz, PhD*
80000
4 pm 4 am
60000 CD63 MFI
78
40000 20000
-4
-3
-2
-1
0
1
2
3
4
5
log (anti-IgE [ng/μl]) Figure 1. Comparison of sensitivity of human basophils at 4 AM and 4 PM. The mean fluorescence intensity (MFI) of CD63 was plotted against the increasing concentration of antihuman IgE. Basophils were significantly more sensitive at 4 PM than at 4 AM (n ¼ 14, P ¼ .0298).
*Department
of Nutritional Medicine University of Hohenheim Stuttgart, Germany y Departments of Clinical Medicine and Respiratory Diseases and Allergy Aarhus University Aarhus, Denmark [email protected]
References [1] Siracusa MC, Kim BS, Spergel JM, Artis D. Basophils and allergic inflammation. J Allergy Clin Immunol. 2013;132:789e801. [2] Boumiza R, Debard AL, Monneret G. The basophil activation test by flow cytometry: recent developments in clinical studies, standardization and emerging perspectives. Clin Mol Allergy. 2005;3:9. [3] Mikkelsen S, Bibby BM, Dolberg MK, Dahl R, Hoffmann HJ. Basophil sensitivity through CD63 or CD203c is a functional measure for specific immunotherapy. Clin Mol Allergy. 2010;8:2. [4] Reppert SM, Weaver DR. Coordination of circadian timing in mammals. Nature. 2002;418:935e941. [5] Durrington HJ, Farrow SN, Loudon AS, Ray DW. The circadian clock and asthma. Thorax. 2014;69:90e92. [6] Baumann A, Feilhauer K, Bischoff SC, Froy O, Lorentz A. IgE-dependent activation of human mast cells and fMLP-mediated activation of human eosinophils is controlled by the circadian clock. Mol Immunol. 2015;64:76e81. [7] Hausmann OV, Gentinetta T, Fux M, Ducrest S, Pichler WJ, Dahinden CA. Robust expression of CCR3 as a single basophil selection marker in flow cytometry. Allergy. 2011;66:85e91. [8] Rorsman H. Normal variation in the count of circulating basophil leucocytes in man. Acta Allergol. 1962;17:49e65. [9] Ando N, Nakamura Y, Ishimaru K, et al. Allergen-specific basophil reactivity exhibits daily variations in seasonal allergic rhinitis. Allergy. 2015;70: 319e322. [10] Santos AF, Du Toit G, Douiri A, et al. Distinct parameters of the basophil activation test reflect the severity and threshold of allergic reactions to peanut. J Allergy Clin Immunol. 2015;135:179e186.
Relationship between maternal and child behaviors in pediatric food allergydan exploratory study Parents play an important role in developing young children’s food choices. They influence children’s eating environments Disclosures: Authors have nothing to disclose. Funding Sources: This study was funded by a studentship of the University of Portsmouth.
through the foods they make available, their own eating behavior, and the quality of their interactions with children in eating contexts.1 In children with food allergies, the development of food habits and preferences takes place in the context of their continuing condition. Mothers often have primary responsibility for the
Letters / Ann Allergy Asthma Immunol 116 (2016) 72e88
dietary management of their child’s allergies in early childhood.2 Although few studies have addressed motherechild interactions in the food allergy literature, research in the pediatric chronic illness literature3 and in the literature with healthy children4 indicate that, in early childhood in particular, developmentally typical feeding difficulties include transient food preferences, picky or fussy eating, and food refusal, which are stressful for parents and a potential cause of interaction difficulties. Collectively these findings point to the importance of redressing the neglect of motherechild interactions in early childhood in the context of food allergies. Research with non-pediatric populations suggests that an authoritative parenting style (high-demanding, high-responsive) promotes healthy food consumption patterns in children5 by providing children with high levels of control and support, and fostering cooperation and self-regulation.6 In contrast, authoritarian (high-demanding, low- responsive), permissive (lowdemanding, high-responsive), or neglectful (low-demanding, low-responsive) parenting styles appear to put children at higher risk for becoming overweight or obese.5 For pediatric food allergy, a child’s cooperation with maternal requests and expectations is particularly important and a positive motherechild interaction style could pave the way for later independent and effective dietary self-management. Thus, this study aimed to compare motherechild interactions of young children with and without food allergies in the context of a novel problem-solving task based on food selection. Participants were children with and without food allergies (4e8 years old) and their mothers. Children with food allergy and their mothers were recruited through an allergy clinic on the Isle of Wight, United Kingdom. Evidence of IgE- or noneIgE-mediated allergy (positive skin prick test or serum specific IgE results plus a convincing clinical history or a positive food challenge result) to egg, milk, peanuts, tree nuts, sesame, crustaceans, fish, or wheat was required. Mothers and children without food allergies were recruited by advertisement on the university Web site. Children were excluded if they had another condition that affected dietary intake. The Southampton and South West Hampshire National Health Service research ethics committee gave this study ethical approval. Initially developed to study motherechild communication in children with diabetes,3 a novel collaborative problem-solving activity involving food shopping and classification for the child’s birthday party was used to compare motherechild interactions of children with and without food allergies. Instructions for the game are presented in Figure 1. Data were analyzed using qualitative ratings of maternal and child behaviors and frequency counts of verbal and nonverbal
79
Figure 1. Instructions for the game.
maternal behavioral control statements. The mothers’ parenting behavior was coded with the Maternal Behavior Rating Scale (MBRS).7 This 12-item scale assesses 4 dimensions of parenting style: responsiveness, affect, achievement orientation, and directiveness. Items include sensitivity to a child’s interest, acceptance, warmth, praise, and pace, and are rated on a 5-point Likert-type scale with ratings of 1 reflecting a low incidence of the quality being assessed and ratings of 5 a high incidence. Parenting categories8 were defined by dichotomizing the sample on each dimension, with the median as the cutoff to categorize into more authoritarian, authoritative, indulgent, and neglecting parent. The children’s interactive behavior with their mothers was coded using the Child Behavior Rating Scale (CBRS),9 which measured 7 global child engagement items: attention, persistence, involvement, cooperation, initiation of activities, joint attention, and affect. Each item also was scored on a scale of 1 to 5. Frequencies of verbal and nonverbal maternal behavioral control statements during the food selection process were coded with the behavior commands (eg, “Take the eggs”), soft directives (eg, “Why don’t we get some chips?”), and requests (eg, “What would you like?” or “What have you put in your
Table 1 Spearman rank correlation coefficients (r) for motherechild behaviors Mother
Sensitivity Responsivity Effectiveness Acceptance Enjoyment Expressiveness Inventiveness Warmth Achievement Praise Directiveness Pace
Child Attention
Persistence
Involvement
Cooperation
Initiation
Joint attention
Affect
0.403 0.321 0.716a 0.391 0.562 0.197 0.451 0.251 0.079 0.296 0.115 0.157
0.004 0.128 0.472 0.164 0.287 0.118 0.050 0.084 0.180 0.138 0.532 0.030
0.446 0.456 0.698a 0.469 0.550 0.230 0.537 0.333 0.049 0.323 0.181 0.029
0.455 0.400 0.776a 0.407 0.637a 0.663a 0.600a 0.813a 0.416 0.596a 0.079 0.157
0.165 0.064 0.404 0.234 0.377 0.057 0.104 0.208 0.134 0.071 0.264 0.175
0.264 0.563 0.875a 0.582a 0.724a 0.836a 0.529 0.712a 0.250 0.800a 0.032 0.173
0.376 0.733a 0.931a 0.713a 0.870a 0.798a 0.622a 0.702a 0.260 0.815a 0.207 0.029
P < .05 (n ¼ 12) for all motherechild dyads combined; mean scores of maternal and child behavior ratings were calculated for correlational analysis; r ¼ 0.60e0.79 indicates a “strong” and r ¼ 0.80e1.0 a “very strong” relation between maternal and child behaviors.
a
80
Letters / Ann Allergy Asthma Immunol 116 (2016) 72e88
basket?”). The key difference among the 3 behaviors is the degree of behavioral control the mother exerts over the child’s food choice decisions. Videotaped observations were coded by the first author and 2 independent raters. Inter-rater agreement was coded according to the formula ([agreements/(agreements þ disagreements)] 100).10 Average inter-rater agreement was initially 68% for the MBRS and 75% for the CBRS before the 3 raters agreed on final ratings for each item. For the frequency coding of maternal control behavioral events, inter-rater agreement exceeded 85%. This study included 12 children, 5 with food allergies and 7 without food allergies. Sample characteristics are listed in eTable 1. For parenting style, no specific pattern for either group emerged. Five mothers used an authoritative parenting style during the activity, 4 an authoritarian style, 2 a neglectful style, and 1 an indulgent style. Four of the 5 children whose mother displayed an authoritative parenting style showed scores above the median with respect to their engagement behavior during the activity. Likewise, food-allergic and nonefood-allergic dyads did not show any differences in their behavior scores (results not presented). Thus, they were combined for further analysis to explore whether there was a relation between maternal and child behaviors that could have clinical relevance for young children with food allergies and their mothers. The analysis of all 12 dyads indicated that mothers who were able to engage the child in the play interaction (effectiveness), clearly enjoyed interacting with the child (enjoyment), communicated and reacted emotionally toward the child (expressiveness), expressed warmth (warmth), and praised the child (praise) had children who were more willing to cooperate with their requests or suggestions (cooperation), initiated interactions and engaged with them (joint attention), and showed positive affect toward the mother or the activity in general (affect). In contrast, mothers who demonstrated more directiveness toward their children (directiveness) appeared to have children who were less engaged in the activity (all dimensions; Table 1). To investigate this trend with respect to the child’s allergic condition, direct counts of maternal control behaviors during the food selection process were performed. Mothers of children with food allergies showed on average a proportionally higher use of commands (18% vs 7%) and soft directives (25% vs 8%) than mothers of children without allergies and they were less likely to utter requests (57% vs 85%). This study concurs with previous research on mothers and their young children with type 1 diabetes3,11 in indicating that the novel approach presented shows promise as a technique for exploring motherechild interactions in young children with food allergy. This approach not only has potential for use as a behavioral assessment tool in clinical settings but can also contribute to future research concerning behavioral aspects of dietary management in young children with food allergies and their parents, especially in combination with complementary research approaches. Results suggest that independent of the allergic condition, mothers who display an authoritative parenting style are more likely to encourage their children to produce high levels of cooperation and positive affect. Such a parenting style could lay the foundation for a favorable relationship toward food by granting children self-regulation and support instead of overprotection and control in relation to their food allergy management. Study limitations include a small sample and findings based on correlational analyses, which preclude insight into causality. These factors limit the
generalizability and conclusiveness of our findings. However, although the findings are of exploratory nature, they could initiate more large-scale research aiming to understand how motherechild interactions in the context of food might influence the long-term management of food allergies in childhood and adulthood. Acknowledgments We thank Jackie Hillman for assistance with data analysis. Supplementary Data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.anai.2015.10.006. Isolde Sommer, PhD*,y Vivienne Chisholm, PhDz Heather MacKenzie, PhDx Carina Venter, PhD*,k Taraneh Dean, PhD*,k *University of Portsmouth School of Health Sciences and Social Work Portsmouth, United Kingdom y Department of Evidence-based Medicine and Clinical Epidemiology Danube University Krems Krems, Austria z Department of Psychology Queen Margaret University Edinburgh, United Kingdom x Graduate School University of Portsmouth Portsmouth, United Kingdom k David Hide Asthma and Allergy Research Centre Isle of Wight, United Kingdom [email protected]
References [1] Mitchell GL, Farrow C, Haycraft E, Meyer C. Parental influences on children’s eating behaviour and characteristics of successful parent-focused interventions. Appetite. 2013;60:85e94. [2] Mandell D, Curtis R, Gold M, Hardie S. Anaphylaxis: how do you live with it? Health Soc Work. 2005;30:325e335. [3] Chisholm V, Atkinson L, Donaldson C, Noyes K, Payne A, Kelnar C. Maternal communication style, problem-solving and dietary adherence in young children with type 1 diabetes. Clin Child Psychol Psychiatry. 2011;16: 443e458. [4] Carnell S, Cooke L, Cheng R, Robbins A, Wardle J. Parental feeding behaviours and motivations. A qualitative study in mothers of UK pre-schoolers. Appetite. 2011;57:665e673. [5] Sleddens EF, Gerards SM, Thijs C, de Vries NK, Kremers SP. General parenting, childhood overweight and obesity-inducing behaviors: a review. Int J Pediatr Obes. 2011;6:e12ee27. [6] Rhee K. Childhood overweight and the relationship between parent behaviors, parenting style, and family functioning. Ann Am Acad Pol Soc Sci. 2008; 615:11e37. [7] Mahoney G. The Maternal Behavior Rating ScaleeRevised. Available from the author; 2008. [8] Maccoby E, Martin J. Socialization in the context of the family: parentechild interaction. In: Handbook of Child Psychology, Volume 4: Socialization, Personality, and Social Development, EM Hetherington, ed. New York: Wiley; 1983, pp 37-51. [9] Mahoney G, Wheeden C. Effects of teacher style on the engagement of preschool aged children with special learning needs. J Dev Learn Disord. 1998;2: 293e315. [10] Bakeman R, Gottman JM. Observing InteractiondAn Introduction to Sequential Analysis. 2nd ed. Cambridge: Cambridge University Press; 1997. [11] Chisholm V, Atkinson L, Bayrami L, Noyes K, Payne A, Kelnar C. An exploratory study of positive and incongruent communication in young children with type 1 diabetes and their mothers. Child Care Health Dev. 2014;40:85e94.
Letters / Ann Allergy Asthma Immunol 116 (2016) 72e88 eTable 1 Characteristics of children
Mean age (y) Sex, n Girls Boys Maternal education, n GCSE or A level Degree level Postgraduate degree level Paternal education, n GCSE or A level Degree level Postgraduate degree level Ethnicity, n White British Black British Asian British Mixed background Type of diet, n Omnivore Vegetarian Culprit foods, n Peanuts Tree nuts Milk Eggs Wheat Avoidance, n Single foods Multiple foods
With food allergy (n ¼ 5)
Without food allergy (n ¼ 7)
5.6
5.1
3 2
5 2
5 0 0
3 1 3
3 1 0
3 2 2
2 1 1 1
7 0 0 0
5 0
7 0
2 1 3 1 2 0 5
Abbreviation: GCSE, General Certificate of Secondary Education.
80.e1
Isotype controls had been used during the validation of basophil activation test. Statistical analyses were performed with GraphPad Prism 6.0 (GraphPad, San Diego, California). Doseeresponse curves were fitted to a 4-parameter nonlinear regression model. Data are presented as mean SEM of 14 subjects. Two-tailed t test for paired samples was used to test for differences between CD63þ cells and CD63 mean fluorescence intensity, respectively, at 4 PM and 4 AM. The significance level was set at P < .05. In this pilot study, we found that basophil sensitivity of volunteers without allergy showed diurnal changes in response to IgEdependent activation. Figure 1 shows a significant decrease in basophil sensitivity at 4 AM (n ¼ 14, P ¼ .0298) when assessed by the mean fluorescence intensity of CD63þ basophils, suggesting that basophils of persons without allergy are less sensitive early in the morning. Notably, we did not find diurnal variation of reactivity assessed by the more commonly used percentage of CD63þ cells in response to anti-IgE at 4 AM and 4 PM (P ¼ .607, data not shown). Hence, our data support the finding that the mean fluorescence intensity is an important parameter in basophil activation test. Mast cells and eosinophils, main effector cells of allergic reactions aside from basophils, recently have been found to exhibit a functional clock mechanism. Clock genes are responsible for generating the circadian rhythm and the clock has been found to control activation of mast cells and eosinophils, resulting in circadian production and release of their mediators.6 These findings assume that the circadian clock influences and controls allergic reactions and not vice versa. Moreover, blood basophil numbers display circadian variations.8 In addition, we found that the intensity of the activation marker CD63 expressed on basophils exhibits diurnal variation. Very recently, daily variations in basophil reactivity have been reported in patients with seasonal allergic rhinitis, with an increase in CD203cþ basophils at 7 AM compared with 7 PM.9 However, we analyzed the circadian rhythm of the sensitivity of basophils of volunteers without allergy. Because donor selection, time points, activation markers, and readout differed between the previous and present studies, the results are not directly comparable. Certainly, further experiments and measurements of more than 2 time points will be necessary to clarify this issue and to explain the higher frequency of allergic symptoms between midnight and morning. At activation, expression of CD63 correlates with degranulation and the release of histamine and with the severity of allergic reactions.2,10 Thus, basophil activation, mediator release, and clock gene expression around the clock and the correlation of circadian allergic symptoms of patients should be analyzed in a follow-up study. In conclusion, this pilot study provides a first hint that the circadian clock might regulate the intensity of basophil response in IgE-dependent allergic reactions. Anja Baumann, PhD* Tina Skjold, MD, PhDy Hans Jürgen Hoffmann, PhDy Axel Lorentz, PhD*
80000
4 pm 4 am
60000 CD63 MFI
78
40000 20000
-4
-3
-2
-1
0
1
2
3
4
5
log (anti-IgE [ng/μl]) Figure 1. Comparison of sensitivity of human basophils at 4 AM and 4 PM. The mean fluorescence intensity (MFI) of CD63 was plotted against the increasing concentration of antihuman IgE. Basophils were significantly more sensitive at 4 PM than at 4 AM (n ¼ 14, P ¼ .0298).
*Department
of Nutritional Medicine University of Hohenheim Stuttgart, Germany y Departments of Clinical Medicine and Respiratory Diseases and Allergy Aarhus University Aarhus, Denmark [email protected]
References [1] Siracusa MC, Kim BS, Spergel JM, Artis D. Basophils and allergic inflammation. J Allergy Clin Immunol. 2013;132:789e801. [2] Boumiza R, Debard AL, Monneret G. The basophil activation test by flow cytometry: recent developments in clinical studies, standardization and emerging perspectives. Clin Mol Allergy. 2005;3:9. [3] Mikkelsen S, Bibby BM, Dolberg MK, Dahl R, Hoffmann HJ. Basophil sensitivity through CD63 or CD203c is a functional measure for specific immunotherapy. Clin Mol Allergy. 2010;8:2. [4] Reppert SM, Weaver DR. Coordination of circadian timing in mammals. Nature. 2002;418:935e941. [5] Durrington HJ, Farrow SN, Loudon AS, Ray DW. The circadian clock and asthma. Thorax. 2014;69:90e92. [6] Baumann A, Feilhauer K, Bischoff SC, Froy O, Lorentz A. IgE-dependent activation of human mast cells and fMLP-mediated activation of human eosinophils is controlled by the circadian clock. Mol Immunol. 2015;64:76e81. [7] Hausmann OV, Gentinetta T, Fux M, Ducrest S, Pichler WJ, Dahinden CA. Robust expression of CCR3 as a single basophil selection marker in flow cytometry. Allergy. 2011;66:85e91. [8] Rorsman H. Normal variation in the count of circulating basophil leucocytes in man. Acta Allergol. 1962;17:49e65. [9] Ando N, Nakamura Y, Ishimaru K, et al. Allergen-specific basophil reactivity exhibits daily variations in seasonal allergic rhinitis. Allergy. 2015;70: 319e322. [10] Santos AF, Du Toit G, Douiri A, et al. Distinct parameters of the basophil activation test reflect the severity and threshold of allergic reactions to peanut. J Allergy Clin Immunol. 2015;135:179e186.
Relationship between maternal and child behaviors in pediatric food allergydan exploratory study Parents play an important role in developing young children’s food choices. They influence children’s eating environments Disclosures: Authors have nothing to disclose. Funding Sources: This study was funded by a studentship of the University of Portsmouth.
through the foods they make available, their own eating behavior, and the quality of their interactions with children in eating contexts.1 In children with food allergies, the development of food habits and preferences takes place in the context of their continuing condition. Mothers often have primary responsibility for the
Letters / Ann Allergy Asthma Immunol 116 (2016) 72e88
dietary management of their child’s allergies in early childhood.2 Although few studies have addressed motherechild interactions in the food allergy literature, research in the pediatric chronic illness literature3 and in the literature with healthy children4 indicate that, in early childhood in particular, developmentally typical feeding difficulties include transient food preferences, picky or fussy eating, and food refusal, which are stressful for parents and a potential cause of interaction difficulties. Collectively these findings point to the importance of redressing the neglect of motherechild interactions in early childhood in the context of food allergies. Research with non-pediatric populations suggests that an authoritative parenting style (high-demanding, high-responsive) promotes healthy food consumption patterns in children5 by providing children with high levels of control and support, and fostering cooperation and self-regulation.6 In contrast, authoritarian (high-demanding, low- responsive), permissive (lowdemanding, high-responsive), or neglectful (low-demanding, low-responsive) parenting styles appear to put children at higher risk for becoming overweight or obese.5 For pediatric food allergy, a child’s cooperation with maternal requests and expectations is particularly important and a positive motherechild interaction style could pave the way for later independent and effective dietary self-management. Thus, this study aimed to compare motherechild interactions of young children with and without food allergies in the context of a novel problem-solving task based on food selection. Participants were children with and without food allergies (4e8 years old) and their mothers. Children with food allergy and their mothers were recruited through an allergy clinic on the Isle of Wight, United Kingdom. Evidence of IgE- or noneIgE-mediated allergy (positive skin prick test or serum specific IgE results plus a convincing clinical history or a positive food challenge result) to egg, milk, peanuts, tree nuts, sesame, crustaceans, fish, or wheat was required. Mothers and children without food allergies were recruited by advertisement on the university Web site. Children were excluded if they had another condition that affected dietary intake. The Southampton and South West Hampshire National Health Service research ethics committee gave this study ethical approval. Initially developed to study motherechild communication in children with diabetes,3 a novel collaborative problem-solving activity involving food shopping and classification for the child’s birthday party was used to compare motherechild interactions of children with and without food allergies. Instructions for the game are presented in Figure 1. Data were analyzed using qualitative ratings of maternal and child behaviors and frequency counts of verbal and nonverbal
79
Figure 1. Instructions for the game.
maternal behavioral control statements. The mothers’ parenting behavior was coded with the Maternal Behavior Rating Scale (MBRS).7 This 12-item scale assesses 4 dimensions of parenting style: responsiveness, affect, achievement orientation, and directiveness. Items include sensitivity to a child’s interest, acceptance, warmth, praise, and pace, and are rated on a 5-point Likert-type scale with ratings of 1 reflecting a low incidence of the quality being assessed and ratings of 5 a high incidence. Parenting categories8 were defined by dichotomizing the sample on each dimension, with the median as the cutoff to categorize into more authoritarian, authoritative, indulgent, and neglecting parent. The children’s interactive behavior with their mothers was coded using the Child Behavior Rating Scale (CBRS),9 which measured 7 global child engagement items: attention, persistence, involvement, cooperation, initiation of activities, joint attention, and affect. Each item also was scored on a scale of 1 to 5. Frequencies of verbal and nonverbal maternal behavioral control statements during the food selection process were coded with the behavior commands (eg, “Take the eggs”), soft directives (eg, “Why don’t we get some chips?”), and requests (eg, “What would you like?” or “What have you put in your
Table 1 Spearman rank correlation coefficients (r) for motherechild behaviors Mother
Sensitivity Responsivity Effectiveness Acceptance Enjoyment Expressiveness Inventiveness Warmth Achievement Praise Directiveness Pace
Child Attention
Persistence
Involvement
Cooperation
Initiation
Joint attention
Affect
0.403 0.321 0.716a 0.391 0.562 0.197 0.451 0.251 0.079 0.296 0.115 0.157
0.004 0.128 0.472 0.164 0.287 0.118 0.050 0.084 0.180 0.138 0.532 0.030
0.446 0.456 0.698a 0.469 0.550 0.230 0.537 0.333 0.049 0.323 0.181 0.029
0.455 0.400 0.776a 0.407 0.637a 0.663a 0.600a 0.813a 0.416 0.596a 0.079 0.157
0.165 0.064 0.404 0.234 0.377 0.057 0.104 0.208 0.134 0.071 0.264 0.175
0.264 0.563 0.875a 0.582a 0.724a 0.836a 0.529 0.712a 0.250 0.800a 0.032 0.173
0.376 0.733a 0.931a 0.713a 0.870a 0.798a 0.622a 0.702a 0.260 0.815a 0.207 0.029
P < .05 (n ¼ 12) for all motherechild dyads combined; mean scores of maternal and child behavior ratings were calculated for correlational analysis; r ¼ 0.60e0.79 indicates a “strong” and r ¼ 0.80e1.0 a “very strong” relation between maternal and child behaviors.
a
80
Letters / Ann Allergy Asthma Immunol 116 (2016) 72e88
basket?”). The key difference among the 3 behaviors is the degree of behavioral control the mother exerts over the child’s food choice decisions. Videotaped observations were coded by the first author and 2 independent raters. Inter-rater agreement was coded according to the formula ([agreements/(agreements þ disagreements)] 100).10 Average inter-rater agreement was initially 68% for the MBRS and 75% for the CBRS before the 3 raters agreed on final ratings for each item. For the frequency coding of maternal control behavioral events, inter-rater agreement exceeded 85%. This study included 12 children, 5 with food allergies and 7 without food allergies. Sample characteristics are listed in eTable 1. For parenting style, no specific pattern for either group emerged. Five mothers used an authoritative parenting style during the activity, 4 an authoritarian style, 2 a neglectful style, and 1 an indulgent style. Four of the 5 children whose mother displayed an authoritative parenting style showed scores above the median with respect to their engagement behavior during the activity. Likewise, food-allergic and nonefood-allergic dyads did not show any differences in their behavior scores (results not presented). Thus, they were combined for further analysis to explore whether there was a relation between maternal and child behaviors that could have clinical relevance for young children with food allergies and their mothers. The analysis of all 12 dyads indicated that mothers who were able to engage the child in the play interaction (effectiveness), clearly enjoyed interacting with the child (enjoyment), communicated and reacted emotionally toward the child (expressiveness), expressed warmth (warmth), and praised the child (praise) had children who were more willing to cooperate with their requests or suggestions (cooperation), initiated interactions and engaged with them (joint attention), and showed positive affect toward the mother or the activity in general (affect). In contrast, mothers who demonstrated more directiveness toward their children (directiveness) appeared to have children who were less engaged in the activity (all dimensions; Table 1). To investigate this trend with respect to the child’s allergic condition, direct counts of maternal control behaviors during the food selection process were performed. Mothers of children with food allergies showed on average a proportionally higher use of commands (18% vs 7%) and soft directives (25% vs 8%) than mothers of children without allergies and they were less likely to utter requests (57% vs 85%). This study concurs with previous research on mothers and their young children with type 1 diabetes3,11 in indicating that the novel approach presented shows promise as a technique for exploring motherechild interactions in young children with food allergy. This approach not only has potential for use as a behavioral assessment tool in clinical settings but can also contribute to future research concerning behavioral aspects of dietary management in young children with food allergies and their parents, especially in combination with complementary research approaches. Results suggest that independent of the allergic condition, mothers who display an authoritative parenting style are more likely to encourage their children to produce high levels of cooperation and positive affect. Such a parenting style could lay the foundation for a favorable relationship toward food by granting children self-regulation and support instead of overprotection and control in relation to their food allergy management. Study limitations include a small sample and findings based on correlational analyses, which preclude insight into causality. These factors limit the
generalizability and conclusiveness of our findings. However, although the findings are of exploratory nature, they could initiate more large-scale research aiming to understand how motherechild interactions in the context of food might influence the long-term management of food allergies in childhood and adulthood. Acknowledgments We thank Jackie Hillman for assistance with data analysis. Supplementary Data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.anai.2015.10.006. Isolde Sommer, PhD*,y Vivienne Chisholm, PhDz Heather MacKenzie, PhDx Carina Venter, PhD*,k Taraneh Dean, PhD*,k *University of Portsmouth School of Health Sciences and Social Work Portsmouth, United Kingdom y Department of Evidence-based Medicine and Clinical Epidemiology Danube University Krems Krems, Austria z Department of Psychology Queen Margaret University Edinburgh, United Kingdom x Graduate School University of Portsmouth Portsmouth, United Kingdom k David Hide Asthma and Allergy Research Centre Isle of Wight, United Kingdom [email protected]
References [1] Mitchell GL, Farrow C, Haycraft E, Meyer C. Parental influences on children’s eating behaviour and characteristics of successful parent-focused interventions. Appetite. 2013;60:85e94. [2] Mandell D, Curtis R, Gold M, Hardie S. Anaphylaxis: how do you live with it? Health Soc Work. 2005;30:325e335. [3] Chisholm V, Atkinson L, Donaldson C, Noyes K, Payne A, Kelnar C. Maternal communication style, problem-solving and dietary adherence in young children with type 1 diabetes. Clin Child Psychol Psychiatry. 2011;16: 443e458. [4] Carnell S, Cooke L, Cheng R, Robbins A, Wardle J. Parental feeding behaviours and motivations. A qualitative study in mothers of UK pre-schoolers. Appetite. 2011;57:665e673. [5] Sleddens EF, Gerards SM, Thijs C, de Vries NK, Kremers SP. General parenting, childhood overweight and obesity-inducing behaviors: a review. Int J Pediatr Obes. 2011;6:e12ee27. [6] Rhee K. Childhood overweight and the relationship between parent behaviors, parenting style, and family functioning. Ann Am Acad Pol Soc Sci. 2008; 615:11e37. [7] Mahoney G. The Maternal Behavior Rating ScaleeRevised. Available from the author; 2008. [8] Maccoby E, Martin J. Socialization in the context of the family: parentechild interaction. In: Handbook of Child Psychology, Volume 4: Socialization, Personality, and Social Development, EM Hetherington, ed. New York: Wiley; 1983, pp 37-51. [9] Mahoney G, Wheeden C. Effects of teacher style on the engagement of preschool aged children with special learning needs. J Dev Learn Disord. 1998;2: 293e315. [10] Bakeman R, Gottman JM. Observing InteractiondAn Introduction to Sequential Analysis. 2nd ed. Cambridge: Cambridge University Press; 1997. [11] Chisholm V, Atkinson L, Bayrami L, Noyes K, Payne A, Kelnar C. An exploratory study of positive and incongruent communication in young children with type 1 diabetes and their mothers. Child Care Health Dev. 2014;40:85e94.
Letters / Ann Allergy Asthma Immunol 116 (2016) 72e88 eTable 1 Characteristics of children
Mean age (y) Sex, n Girls Boys Maternal education, n GCSE or A level Degree level Postgraduate degree level Paternal education, n GCSE or A level Degree level Postgraduate degree level Ethnicity, n White British Black British Asian British Mixed background Type of diet, n Omnivore Vegetarian Culprit foods, n Peanuts Tree nuts Milk Eggs Wheat Avoidance, n Single foods Multiple foods
With food allergy (n ¼ 5)
Without food allergy (n ¼ 7)
5.6
5.1
3 2
5 2
5 0 0
3 1 3
3 1 0
3 2 2
2 1 1 1
7 0 0 0
5 0
7 0
2 1 3 1 2 0 5
Abbreviation: GCSE, General Certificate of Secondary Education.
80.e1