La tunisie Medicale - 2018 ; Vol 96 ( n°07 ) : 417-423
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INTRODUCTION: Les facteurs psychologiques et l'environnement familial peuvent jouer un rôle dans la pathogénie et la persistance des symptômes de la dermatite atopique (DA). L'objectif de notre étude était d'évaluer les interactions entre les mères et leurs enfants souffrant de DA et de rechercher la présence de dépression et d’anxiété maternelles.
MÉTHODES: Un échantillon de 24 enfants atteints de DA et de leurs mères et 24 dyades témoins appariés ont participé à l'étude. La dépression maternelle et l'anxiété ont été évaluées à l'aide de l'Inventaire abrégé de la dépression de Beck (BDI) et l'échelle d'évaluation de l'anxiété de Hamilton (HAM-A). L'interaction mère-enfant a été évaluée par enregistrement vidéo et par des scores établis après analyse de la vidéo: M-score pour l'attitude de la mère envers l'enfant et C-score pour le comportement de l'enfant.
RÉSULTATS: les mères du groupe DA ont affiché des scores significativement plus élevés sur le HAM-A, mais pas sur le BDI. L'analyse de l'enregistrement vidéo a révélé une différence significative dans les scores M entre les deux groupes, mais aucune différence dans les scores C. Le score M a été corrélé à l'anxiété de la mère.
CONCLUSION: Notre étude a révélé des arguments en faveur d'une perturbation de l'interaction mère-enfant dans le groupe DA notée du côté de la mère,avec plus de symptômes d'anxiété de la mère que le groupe témoin. Nos résultats suggèrent la nécessité d'un soutien psychologique pour les mères d'enfants atteints de DA.

Mots Clés

Atopic dermatitis (AD) is a relatively common inflammatory disease of childhood. Its prevalence within the pediatric population has increased during the past three decadestocurrently15%to20%(1).However, studies in certain developing countries like Tunisia found a prevalence of less than 1%(2, 3). ThemainsymptomofADisitchiness,resulting in damage to the skin due to scratching of the afflicted area.

Several factors are involved in the genesis and exacerbation of AD: genetic, environmental,andpsychologicalfactors; some authors underlined the relationship between stress, anxiety and immune dysregulation in AD(4, 5). Moreover, there seems to be a link between stress,family environment,stylesoffamilyinteractionandsymptomseverityinchildrenwithAD(6). A recent study showed that maternal post partum depression increased the risk of childhood AD (7).
The relationship between early parent-child interaction and chronic disorders in infants seems to be of particular importance, but few studies have been conducted in this area(8-12). Anxiety, depression or other emotional states in the parents can influence the quality of parent-child interactions(13). Similarly, thebehavior and disorders of the child may interfere with the parent-child relationship.
The caregiver-child interaction has been reported as a reciprocal process with each partner influencing the other(14). Disturbance of the parent-child relationship may be due to either partner. It may be due to the childbeing unrewarding, little smiling and often crying, as noted by a study that explored the perception of the temperament of the AD infant by their mother(8).Ontheparent’sside,exhaustionduetothechild’sdisease,negative affectivity such as depression, guiltiness, anxiety may negatively interfere with the parent-child interaction.
Studies on parental characteristics and educative style in AD children yielded contradictivefindings.AstudybyRingandPalos,exploring several aspects of the parent-child relationship in AD, suggests that mothers of atopic children are less “spontaneous”, more “undercontrol”, “distant” and less “emotional”, as well as “stricter” in their educational approach, compared to controls(9, 10). However, a replication study with a larger sample size failed to confirm these findings, and a study on psychosocial adjustment in preschool children with AD reported positive affective responses towards the child and even maternal permissiveness(15). Pauli-Pott et al reports in her study a more “anxious overprotectiveness” but not more “rigidity” in child rearing attitudes of mothers of AD children compared to controls(8).
According to several studies, rearing a child with AD might not only influence educative style, but puts enormous strain on the parents(8, 11, 16). The study by Manzoni showsthatanxiety anddepression wereobservedin36%ofcaregiversofpatientswithAD(17).

The aim of our study was to examine the differences in interaction between dyads of mothers and their children suffering from AD and healthy dyads and to explore anxiety and depression in mothers.

We conducted a cross-sectional case-control studybetween February and June 2010. The local ethics committee approved the study. All the mothers who participated in the study provided their consent after being informed of the purpose and the conduct of the study.
Atotalofforty-eightmother-childdyadsparticipatedinthestudy.Weincluded twenty- fourchildrenwithADmonitoredinthedepartmentofdermatologyatCharlesNicolle HospitalinTunis, Tunisia.ExperienceddermatologistsconfirmedtheADdiagnosisaccording to the criteria established by Hanifin and Rajka(18). As control subjects, we recruited twenty-four mother-child dyads from a maternal and child health center in the district of Tunis, where vaccination and routine examination of children are performed. All participating children were aged less than 36 months.For the index cases, we excluded children with other non-atopic conditions associated with AD.Healthycontrolchildrenhadtobefreeofchronicdiseases especiallyatopicdiseaseandrespiratorydisease.Thecontrolsubjectswerematched accordingtoageandsex.
Assessment and Procedure

Theassessment was conducted in one session which consisted of two parts: 1) a video recording of the mother-child dyad, 2) an interview with the mother also comprising the administration of ratingscales to the mother. Two child and adolescent psychiatrists conducted interviews and provided interpretations of the video.
ThedermatologistwasaskedtocompleteananamnesticquestionnaireabouttheAD comprising localizations of eczematous lesions, signs of pruritus and course of the disease. AD severity was assessed by SCORAD(19). We considered AD to be mild whentheSCORADscorewaslowerthan20,moderatewhenSCORADwasbetween 20 and 39, and severe when the SCORAD score was 40 or more.

Thevideorecordingofthemother-childdyadtookplaceduringtheconsultationwith thedermatologistfortheADgroupandduringtheroutinemedicalconsultationforthe control group. At the end of the consultation, mothers were asked to apply a neutral moisturizer cream to the body of their children. During the application of the cream, mother and child were filmed for three minutes. The forty-eight video analyses were performed separately by two child and adolescent psychiatrists (A.B. and E.F.J.) who were specially trained on the subject, and one of whom is specialized in infant psychiatry. Theratersofthevideoswereblindedregardingthegroups(ADversuscontrols).The videoswereanalyzedaccordingtoaratinggriddevelopedbytheauthors.Incaseof discrepancy between the two raters, the video was revisited and analyzed asecond time by the two raters together. The rating grid contained two items for reaction and attitude of the mother and the baby during the medical examination. The baby's reaction was assessed according to: “no reaction”, “seeks interaction with the mother”,“seeksinteractionwiththedoctor”,“anxiousabouttheexamination”or“other reactions”. The mother’s reaction was assessed according to “especially interested in the medical examination” or “interested in maintaining contact with the child”.
Fortheitemsconcerningtheapplicationofthecream,weestablishedtwoscores:the first regarding mother’s attitude towards the child (“M-score”) and the second regarding the child’s behavior (“C-score”). The M-score varies from 0 to 8: a higher score indicating an inadequate attitude of the mother within the dyad. The C-score varies between 0 and 6, a higher score indicating a distress reaction of the child (Appendix).Wenotedtheitemcharacteristicorcategory,whichwasexhibitedbythe mother or by the child approximately 50% or more of the video recording time. The internal consistency of both Mother’s attitude including mother items and Child Behavior including child items was measured by Crohnbach’s alpha. It was 0.85 for Mother’sattitudeand0.47forChildBehavior.
Theinterviewwasconductedwiththehelpofastructuredquestionnaire.Itcontained data on socio-demographic characteristics, antenatal and perinatal period, psychomotor development of the child, duration of breastfeeding, child’s sleep,and type ofchildcareandmedicalhistoryofeachparent.Allmotherswerethenscreened fordepressionandanxietyusingtheBeckDepressionInventory–shortform(BDI)in its Tunisian-Arabic version and the Hamilton Anxiety Rating Scale (HAM-A)translated into Tunisian Arabic(20). The short form of the BDI consists of 13 items,each one scored from 0 to 3, indicating increasing depressive symptom severity. TheHAM-A includes 14 items, comprising psychological and somatic symptoms, each one rated from 0 to 4. It evaluates the present and the past week’s symptoms(20).
Statistical analysis

StatisticalanalyseswereconductedusingtheStatisticalPackageforSocialSciences Version 18. Analyses compared the 24 dyads with AD children with the 24 control dyads. Chi-square test was used to compare qualitative variables. Quantitative variables were compared by the t test of Student. Pearson correlation analysis was carried out to explore the associations between quantitative variables. We establishedthelevelofsignificanceatα=0.05.

Thesocio-demographiccharacteristicsofthetwogroupsaresummarizedinTable1. No significant differences for the general characteristics between the two groups were found.
We found a history of asthma and bronchiolitis in three children with AD out of 24. MothersofchildrenwithADhadasignificantlyincreasedpersonalhistoryofphysical diseases(p<0.01),amongstthemninecasesofallergyandasthma.Themothersof the control subjects had no history of atopic disease or skin disease. Medical history but no atopic disease was found in five fathers of the clinical group and four fathers of the control group without differences between the twogroups.Theparentsinthetwogroupsdidnotreportanyhistoryofpsychiatricillness.
The results concerning pregnancy, perinatal period and child development are summarized in Table 2. There were no significant differences between the two groupsregarding the mothers’ desire for pregnancy, the course of pregnancy, the perinatal period, breastfeeding and its duration, the child’s sleep and child development.
As to severity of AD defined by SCORAD, 17 children had moderate and sevenchildrenhadmildAD.ThemeanSCORADscorewas23.15(standarddeviation7.32; rangesfrom8.8to38.3).
During medical examinations, reactions and attitudes of the mothers were significantly different between the two groups. Mothers of AD children were more interested in the medical examination, whereas mothers of healthy children usually kepttheirfocusontheirchildren(19/24vs5/24)(p<0.01).Thechild’sreactionswere also significantly different between the two groups (p<0.001). Thus, anxiety was found in 11/24 AD children versus 1/24 children in the control group. Seeking interactionwiththemotherand/ortheexaminerwasfoundin7/24ADchildrenversus 19/24 controls, and no reaction was observed in 6/24 AD children versus 4/24 controls.
ComparisonofM-scoresbetweenthetwogroupsshowedasignificantdifference(p< 0.001),whereastherewasnosignificantdifferencebetweentheC-scoresofthetwo groups (Table 3).
There was no significant difference in depression scores between the two groups (Table3).However,mothersof the AD group exhibited considerably more anxiety symptoms than mothers of the control group(p<0.01)(Table3).
Both M and C-scores were significantly positively correlated with the HAM-A (with respectively r= 0.41, p<0.01 and r=0,32 p<0.05). C-scores were also correlated to BDI score (r=0.29 p<0.05). No significant correlation was found between M-scores and BDI and between M and C-scores and the SCORAD (Table 4).

Discussion and Conclusions

Theimportantfindingofourstudyisthecleardifferenceinthequalityof the mother-child interactionbetweentheADandthecontrolgroup,duringmedicalexaminationaswell asduringapplicationofthecream.Indeed, mothersofADchildrenshowimpairedskin-to-skincontact, less eye contact, and less vocalizations with their children. To our knowledge, this is the first Tunisian study examining the mother-child-interaction in the context of chronic disease and the mental health of the parents.

OurresultsshowedthatmothersofADchildrenhadsignificantlymoreanxietybutnot significantly more depressive symptoms compared to mothers of healthy children. Ourfindingsconfirmtheresultsofthefewstudiesconductedinthisareaandinwhich mothersofADchildrenexhibithighlevelsofanxiety(8, 17).Incomparisonwithprevious studies, we did not find an association between depression and mother’s behavior(8, 17).Thisisprobablyduetolackofpower.
Two recent studies show links between maternal stress at preconception and AD risk at 12 months as well as maternal stress and anxiety at delivery, pointing to a developmental contribution to the occurrence of AD(21, 22).A systematic review suggests a relationship between maternal stress during pregnancy and atopic disorders in the child(23).

The high frequency of anxiety symptoms in the AD mothers group of our sample might be explained by feelings of uncertainty and negative anticipation about the furthercourseoftheillness,guiltinessforhavingtransmittedageneticpredisposition to the child, grief about the external appearance of the child, which may be unattractiveduetotheskinlesions,ortheincreasedneedsofthechildforcareand parental involvement(8). A recent study found that mothers of AD children exhibited less affection and more rejecting attitudes towards their child (24). Another study with 242 mothers and their infants with AD showed that higher maternal controlling behaviors and unresponsiveness predicted greater odds of AD(25).

Thelevelofmother’sanxietywassignificantlycorrelatedtobothMandC-score.The presence of anxiety symptoms in the mothers of AD children may influence their behavioral interactions with the child. In our study, the inappropriate maternal interaction with the child in the AD group might therefore be explained by the significantlyelevatedlevelsofanxietyinADmothers.
The disturbance in the parent-child-interaction could also be caused by the child sufferingfromAD.Indeed,thereisahighriskthatachronicillnesslikeADmightlimit oralterthechildren’scommunicativebehaviorsandimpactonthechild’spersonality. In our study, the AD children showed more distress and less interaction seekingduring the medical examination, but we did not find a difference between AD andcontrol group children during the application of the cream. This difference notedduring the medical examination could be explained by the circumstances of the examination that might have been inherently more stressful to the AD children. The lower interaction seeking could be a response to the mother’s low affective availabilitytotheADchildduringtheexamination,themotherbeingmoreinterested in the medical examination than in the child. In the Pauli-Pott study, mothers characterized their infant suffering from AD as significantly less frequently positive andmorefrequentlynegativeinitsemotionalbehaviorcomparedtothecontrol group(8). Preschool children with AD exhibited more frequently behavioral symptoms, with a significant excess of dependency and clinginess, fearfulness and sleep difficulty(15). A study by Cassibba et al on a group of 10 premature and 10 AD infants and a control group of 20 full term and healthy infants shows a high incidence of insecure infants in the clinical group (AD infant and premature infant) evaluated by the strange Situation Procedure(12).A study on 64 parent-child dyads with AD showed that parents of children with more severe AD were responding to difficult child behavior less appropriately, potentially impacting on illness management(26).
Giventhecross-sectionaldesignofourstudy,itisnotpossibletodeterminewhether the disturbance in the mother-child relationship is a precursor or a result ofthe disease. Many studies have shown that the psychological development of the baby depends largely on positive andstable interactions(13).  Given the context of our study, we hereby only illustrate the importance of touch: From a psychological point of view, skin stimulation helps with the development of body imageand self-esteem(27). Several studies examining the infant’s reaction to touch stimulation showed more smiling and vocalizing and less distress in infants who received touch from their mothers(28-30). Reduced maternal interaction with the child might increase the child’s distress and lead to a less secure attachment,whichinturnmakesthechildmorevulnerabletostressors.Psychosocial stress and skin condition share a bidirectional relationship. Stress exacerbates AD, and the worsening of AD lowers the stress threshold(31). This means that there might beahigherriskforADtopersistwhenthemother-childinteractionisdisturbed.

Ourstudyhasthefollowinglimitations:Thesamplesizewasestablishedempirically, without conducting a power analysis. The observation took place during and after the medical examination, a situation probably more stressful for the AD group. The observation time during the application of the cream wasrelativelyshort.Alongerobservationtimeandtheuse ofseveralcamerasinsteadofasinglecamerawouldhaveimprovedtheevaluationof themother-childinteraction.Althoughtheratersofthevideoswereblindedregarding the group (AD versus controls), there was a risk that the children suffering from AD would be identified in the video given that the skin lesions might be apparent. Furthermore, the Arabic versions of the HAM-A and the BDI scale arenotyet validated.
Futurestudieswithlargersamplesizesare neededtoconfirmourfindingsand togetamorein-depthviewofthecausalityofthe disturbedmother-child interaction. The objective would be to propose adequate psychological care to the parent-child dyads. Some observational case studies  suggest  that  treatments  aimed  at  improving the  parent-childinteraction improve  both  skin  and  behavioral  symptoms(32, 33).  Multidisciplinary care programs including support for parents of the affected childrenhave shown to improve coping with AD and quality oflife(34, 35).
In conclusion, the results of the present study provide evidence that the mother-child interaction is clearly disturbed and that maternal anxiety is more frequent in the case of the child suffering from AD. However, we could not determine whether the disturbance in the mother-child relationship was a precursor or a result of the disease. Our findings underline the need for psychological support for mothers of children with AD..

Table 1: Socio-demographic characteristics of dyads with AD child and controls

Table 2: Pregnancy, perinatal period and child development

Table 3: Results of M-score, C-score, Beck DepressionInventory and Hamilton Anxiety Rating Scale

Table 4: CorrelationsbetweenHAM-Ascore,BDIscoreand SCORADwith“M- score”and “C-score”

Appendix:M-ScoreandC-Scorerating of thevideorecordingduringtheapplicationof thecream

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