See “Thinking Outside the Box When Dealing With Patients With GERD and Feeding Problems” by Lifschitz on page 358.
Gastroesophageal reflux (GER) is the movement of gastric contents into the esophagus. In most infants, GER is an uncomplicated self-limiting condition that resolves with age (1). In more severe cases, it can be associated with respiratory symptoms and feeding problems (2,3); when the reflux of gastric contents causes problematic symptoms and/or complications, the condition is called gastroesophageal reflux disease (GERD) (4). Feeding problems reportedly observed with GER include odynophagia (5), dysphagia (6), resistance and aversion to feeding (7), and excessive crying and irritability related to feeding (8).
According to the Chatoor classification of feeding disorders, GER belongs to the group of feeding disorders associated with concurrent medical conditions (9). One of the diagnostic criteria of this group of patients is that medical management improves but does not fully alleviate feeding problems because of the interaction between organic and psychological factors that lead to such problems in the first place. Among these psychological factors, maternal factors such as the mother's ability to understand the clues given by the child are important for the development of healthy feeding patterns. Maternal psychopathology can lead to misinterpretation of these clues and impair mother–child interactions (10). Dellert et al (7) identified the importance of impairment in mother–child interactions in the perpetuation of feeding difficulties in GER; they found a high level of maternal worrying and severe frustration at feeding time in families of infants with GER. The relation between feeding problems in children with GER and maternal psychopathology is poorly documented, however. Although some studies reported that GER is associated with maternal anxiety and depression (11,12), these studies have methodological limitations: the diagnosis of GER was not confirmed in all of the cases, comparison groups were not used, and the aspects of psychopathology other than anxiety and depression and the effects of maternal psychopathology on feeding problems were not assessed. Furthermore, maternal psychopathology was not assessed in the only controlled study investigating the feeding problems of infants with GERD (13).
The present study was conducted to identify the effects of maternal psychopathology on the feeding problems in children with GERD and the effects of GERD on the psychomotor development of children. Two hypotheses were tested: maternal psychopathology is high in mothers of children with GERD and can be related to feeding problems, and GERD has an effect on the psychomotor development of children. To test the first hypothesis, we aimed to extend the existing knowledge about maternal depression and anxiety and to assess 2 other aspects of maternal psychopathology: disturbed eating attitudes and attachment. To test the second hypothesis, we assessed the psychomotor development of children with GERD by using a developmental test that measures the motor and mental development of children.
SUBJECTS AND METHODS
The inclusion criteria for the case group were age between 2 and 36 months and a diagnosis of GERD confirmed by the authors (specialists in pediatric gastroenterology) on the basis of history and/or 24-hour pH monitoring. GERD was defined as the reflux of gastric contents, which causes troublesome symptoms and/or complications. GERD was diagnosed whenever an association among symptoms, signs, and reflux events in the absence of alternative diagnoses was documented by history, physical examination, and pH metry (according to established criteria) in cases where needed (4). Twenty-four-hour pH monitoring was needed in cases wherein GERD diagnosis could not be confirmed on the basis of medical history or when the medical history was atypical of GERD but GERD was suspected on the basis of the child's clinical progress. The exclusion criteria were the presence of a physical disease other than GERD or a pervasive developmental disorder that may affect several aspects of the relationship between the child and mother, including feeding. All of the patients seen for GERD who did not have a physical disease apart from GERD and were between 2 and 36 months of age were referred to the psychiatrist by the pediatric gastroenterologists between April 2006 and March 2010; as part of the study, the children were assessed by the psychiatrist. The study was approved by the ethics committee of Cerrahpasa Medical Faculty.
Children were included only after their parents gave written informed consent to participate in the study. Comparison infants were recruited from the well-baby clinic of Cerrahpasa Medical Faculty. The children in the case and comparison groups were matched in terms of age, gestational age, socioeconomic status, and sex.
A general data form was developed by the authors that included questions about the age and level of education of the mothers; whether conception was planned; complications in the prenatal, perinatal, and postnatal periods; gestational age; type of delivery; birth weight; duration of breast-feeding; presence of crying spells; age at GERD diagnosis; and feeding patterns. The questions asked to assess feeding concerned food refusal, appetite, feeding while asleep, feeding between meals, the child's distress at feeding time, maternal thoughts of the child's feeding as insufficient, forced feeding, vomiting after forced feeding, autonomy of the child about feeding, and the mother's support of autonomy of the child about feeding. As stated above, food refusal was defined as the child spitting out food, gagging, or dawdling (extended or easily distracted while feeding) (14). Children were diagnosed as having failure to thrive (FTT) when their growth slowed or when the arrest in growth resulted in a reduction in the weight and height measurements to a value less than the third percentile on the standard growth curve across 2 major percentiles over time (15,16). The scales used for psychiatric assessment of the mothers were the Beck Anxiety Inventory (BAI), Hamilton Rating Scale for Depression (HAM-D), Eating Attitudes Test (EAT), and Experiences in Close Relationships-Revised (ECR-R).
BAI is a 21-question self-report scale. Higher scores are correlated with more severe anxiety symptoms (17). The reliability and validity of the BAI for the Turkish population were confirmed by Ulusoy et al (18).
HAM-D is a 17-item clinician-rated questionnaire that rates the severity of depression symptoms (19). A total score ≤7 may be considered normal; 8 to 13, mild depression; 14 to 18, moderate; 19 to 22, severe; and ≥23, very severe (20). The reliability and validity of this scale for the Turkish population were confirmed by Akdemir et al (21).
EAT is a 40-item self-report questionnaire that has a cutoff point of 30 (22). The reliability and validity of the EAT for the Turkish population were confirmed by Savasir and Erol (23).
ECR-R is a 36-item self-report scale that measures attachment in 2 dimensions: avoidance and anxiety (24). The reliability and validity of this scale for the Turkish population were confirmed by Selcuk et al (25). Secure attachment was defined as mothers who had low scores in both attachment-related anxiety and avoidance. Insecure attachment was defined as mothers who had a high score in attachment-related anxiety or avoidance, as defined previously (26).
The developmental levels of children were assessed by the Brunet-Lezine-Revised (BL-R) test, a developmental test that measures the motor and mental development of children between 2 and 30 months. It can also be used for children older than 30 months if their retardation results in failure to accomplish developmental milestones within 30 months of age. The BL-R consists of 4 subscales that screen posture, language, socialization, and coordination. The reliability and validity of this test for the Turkish population were confirmed by Kayaalp et al (27).
Categorical variables were compared using the χ2 or Fisher exact test; the ordinal or score variables were compared using the Mann-Whitney U test. The Student t test was used to compare quantitative variables. The data were analyzed using the SPSS 16-pocket program (SPSS Inc, Chicago, IL). The level of significance was set at P < 0.05 for all of the tests. In addition, binary logistic regression analysis was used to assess the relation of maternal assessments and feeding parameters with GERD. The variables that produced P values of <0.1 in univariate analysis were assessed in different models by binary logistic regression analysis based on whether the variable was calculated from the case or comparison group. As a result, a model was constructed with the following variables: maternal HAM-D, EAT, and BAI scores; the type of delivery; presence of crying spells; distress during feeding; maternal thoughts of the child's feeding as insufficient; forced feeding; and food refusal.
The ages of the children in the case and comparison groups ranged from 4.7 to 34 months and 4.33 to 29 months, respectively. The mean ages of the children in the case and comparison groups were 15.62 and 15.67 months, respectively (not statistically different). The case group consisted of 39 children with GERD and their mothers, and the comparison group included 39 healthy children and their mothers. There were 26 boys and 13 girls in each group. Both groups included 7 children who had a premature birth. Table 1 shows the characteristics of the children. Among the sociodemographic parameters, only the type of delivery differed between groups, with the case group having more cesarean deliveries. There were no significant differences between the groups in terms of maternal age or education; whether the conception was planned; prenatal, perinatal, and postnatal complications; birth weight; and the duration of breast-feeding (Table 1). The birth weights (mean ± standard deviation) were 3208.97 ± 753.35 g and 3304.36 ± 778.61 g in the case and comparison groups, respectively. The mean duration of breast-feeding was 6.96 ± 5.97 months and 8.69 ± 5.71 months in the case and comparison groups, respectively. Age at the time of GERD diagnosis ranged from 1.16 to 33.83 months with a mean of 11.58 months. The duration of GERD ranged from 15 days to 17 months with a mean of 4.05 months.
Statistically significant differences were found between the 2 groups with respect to food refusal, distress during feeding, forced feeding, vomiting after forced feeding, poor appetite, and the mother's thoughts of the child's feeding as insufficient (Table 2). The majority of the case group (n = 24, 61.5%) vomited more than once per day, whereas the rest (n = 15) vomited once per day. None of the children in the case group was vomiting less than once per day. The case group consisted of 11 children with FTT. Thirty-one children exhibited irritability during the psychiatric interview, and 29 of them were reported by their mothers to be distressed during feeding. Crying spells were found in 22 of the children with GERD and 11 of the comparison group (P = 0.012). There were no significant differences between the 2 groups in terms of feeding between meals, feeding while asleep, autonomy about feeding, and maternal support of autonomy about feeding.
Maternal assessments revealed statistically significant differences between the 2 groups with respect to BAI, HAM-D, EAT, and ECR-R scores (Table 3). Seventeen (43.58%) mothers had EAT scores of >30, which suggests that they have disturbed eating attitudes. When the relation between maternal scales and feeding problems was analyzed by the Mann-Whitney U test, maternal thoughts of the child's feeding as insufficient were significantly associated with ECR-R anxiety (P = 0.032) and avoidance scores (P = 0.016). Forced feeding was associated with ECR-R anxiety (P = 0.028) and avoidance scores (P = 0.047). Food refusal was not associated with any maternal psychiatric assessment but coexisted with forced feeding (P = 0.001), vomiting after forced feeding (P < 0.001), distress during feeding (p = 0.002), and maternal thoughts of the child's feeding as insufficient (P = 0.036). The mother's thoughts of the child's feeding as insufficient coincided with forced feeding (P = 0.011) and distress during feeding (P = 0.002). The relation between the age of the children with GERD and the maternal BAI, HAM-D, EAT, and ECR-R scores was assessed by calculating the Spearman rank correlation coefficient; this revealed a moderate but significant correlation between ECR-R–anxiety subscale scores and children's ages. This correlation between age and the ECR-R–anxiety subscale scores was unidirectional (rs = 0.46, P = 0.003). All of the other maternal assessments, including the BAI, HAM-D, EAT, and ECR-R avoidance subscale scores, were not significantly correlated with the age of the children. In addition, no significant correlation was found between maternal assessments, including the BAI, HAM-D, EAT, and ECR-R scores, and the age of the children of the entire sample (ie, both case and comparison groups). Logistic regression analysis indicated food refusal (P = 0.002; odds ratio [OR] 8.47), EAT scores (P = 0.005; OR 1.163), and HAM-D scores (P = 0.024; OR 1.291) were associated with GERD.
Eleven children in the case group had FTT. When the case group was subdivided according to the presence of FTT, the association of FTT with maternal psychiatric problems was assessed; the ECR-R–avoidance subscale was found to be associated with FTT (P = 0.031). When depressed mothers were subdivided into 2 groups according to the severity of depression (mild–moderate and severe–very severe), the severe to very severe group coexisted with vomiting after forced feeding (P = 0.042) and maternal thoughts of the child's feeding as insufficient (P = 0.024).
As a result of developmental assessment, significant differences between the 2 groups in all of the subscales and the total scores of BL-R were found (Table 4). Among the subscales, language and socialization had the lowest mean scores.
One child in the case group who was 34 months and 25 days old failed to accomplish developmental milestones by 30 months; therefore, we could determine his psychomotor delay by using BL-R.
To the best of our knowledge, this is the first case-control study investigating the maternal psychopathology and the psychomotor development of children with GERD. Food refusal was the most common feeding problem in the case group; this finding is consistent with a study in which food refusal was the most common feeding problem (with a prevalence of 95%) in a population of children referred to a feeding program (28). Previous studies define food refusal in a variety of ways. Some authors describe it as a general term encompassing a wide range of feeding problems (29), whereas the others define it in terms of decreased appetite (30). Furthermore, it is also defined as a more specific type of feeding problem characterized by a child's complete or partial refusal to eat the foods presented to him or her, resulting in a failure to meet his or her energy and/or nutritional needs (31). In our study, we referred to the definition of food refusal by the presence of behaviors such as spitting out food, gagging, or dawdling (14). Previous studies found food refusal to be associated with GERD (7,13,31–33); however, these studies poorly document its association with maternal factors. It is suggested that poor gastric emptying may manifest as early satiety during feeding, and that continued efforts to feed after the infant reaches satiety may be associated with discomfort and negative reinforcement toward feeding (7). Our study supports this idea in that food refusal coexisted with forced feeding, vomiting after forced feeding, and distress during feeding. Forced feeding was among the abnormal parental feeding practices that Levy et al (33) found to be one of the diagnostic clues discriminating nonorganic causes of food refusal. In the present study, forced feeding was common in the nonorganic food refusal group, which included children without underlying disorders as well as children with additional medical pathologies who were unresponsive to medical, nutritional, or surgical interventions but subsequently responded to behavioral intervention. In the same study, 20.5% and 29% of the patients in the nonorganic and organic food refusal groups, respectively, had GER (33). In our study, there was no association between food refusal and maternal psychopathology; this finding is inconsistent with that of Lindberg et al (14), who found a high level of parental anxiety and depression in children with food refusal. The present study is consistent with the findings of Coulthard and Harris (34), who found no difference between maternal anxiety and depression scores in children exhibiting food refusal. Lindberg et al (14) concluded that maternal negative perceptions of parenting could be a perpetuating factor in the development or maintenance of food refusal. Although maternal perceptions about parenting were not assessed in our study, we can conclude from our findings that maternal insecure attachment via forced feeding can lead to impairments in mother–child interactions and that forced feeding in turn results in food refusal.
FTT was found in 11 (28.2%) of cases in the present study. Previous studies report both higher (57%) (35) and lower (18%) (8) ratios of FTT in children with GER. These differences may be because of the characteristics of the study populations: the former study included treatment-resistant cases and the latter included children who were younger than those in our case group. Because the children in our study were older at diagnosis than those in the study by Shepherd et al (8), they had time during which they experienced untreated reflux and its complications that affect growth, such as FTT. GER is known to occur more frequently in the early periods of infancy (36).
When the case group was subdivided according to the presence of FTT and the association of maternal factors with FTT was assessed, the attachment-related avoidance subscale was found to be associated with FTT. This is consistent with studies that found an association between insecure attachment and FTT (37). Benoit et al (37) suggest that insecure attachment is a causal factor of a disordered relationship between mother and infant, which, in turn, contributes to FTT. Our findings suggest that insecure attachment is associated with forced feeding, which coincides with food refusal, which, in turn, may be a mechanism leading to FTT. The lack of association between FTT and maternal depression found in the present study is inconsistent with some (38) but consistent with other previous studies (39). Because feeding is considered one of the most important ways in which parents communicate with their infants (40), the mother's own attachment, which primarily influences mother–infant communication (41), should be evaluated when assessing feeding problems. Although insecure attachment is reported in adults with GER (42), the attachment patterns of mothers of children with GERD were not previously studied.
In terms of depression, our findings are consistent with those of previous studies that found an association between maternal depression and GER (11,12). Because the diagnoses of GER and depression were not confirmed in all of the cases in these studies, the association could not be confirmed. We did not find a statistically significant relation between depression and feeding problems. When mothers in the case group were subdivided according to the severity of depression, however, it could be concluded that maternal depression interferes with the feeding process; this probably occurs because of blunting the responsiveness of the mother to her child, increasing severity of depression coexisting with thoughts that her child is not being sufficiently fed, which, in turn, results in vomiting after forced feeding.
Maternal anxiety was significantly more prevalent in the case group than in the comparison group. Although maternal anxiety was not assessed previously, maternal distress (8) and the components of maternal feeding anxiety, such as becoming upset when the infant does not eat (32), are reported to be common in GER. Maternal feeding anxiety is defined as maternal stress during mealtimes and worrying about the child's feeding (43). In our study, a significantly higher number of mothers in the case group reported that they considered their child's feeding as insufficient. This idea, which can be interpreted as a sign of maternal feeding anxiety (43), coincided with forced feeding, which explains how maternal feeding anxiety disturbs feeding. In addition, as seen in Table 2, forced feeding was observed even among controls and in the mothers of children who do not refuse to eat. This fact may be attributable to cultural factors affecting feeding practices. In Turkish culture, babies who have big appetites and are overweight are considered healthy, whereas babies who do not have big appetites and are lean are considered unhealthy and are a source of concern for their mothers (44). This cultural aspect can lead to maternal anxiety during mealtimes and forced feeding even if the child does not refuse to eat. We found that mothers of the children with GERD differed significantly from the comparison group in terms of eating attitudes. There was no significant association between maternal disturbed eating attitudes and forced feeding; however, a high proportion of mothers of children with GERD who were forcing their child to eat had disturbed eating attitudes themselves (48.3%). An even higher proportion of mothers of children with GERD who had disturbed eating attitudes were forcing their child to eat (88.2%). This finding is consistent with that of Stein et al (40), who found that mothers with eating disorders are more intrusive, are less facilitating, and manifest more conflict during mealtimes than are controls.
Children with GERD had significantly lower total and subscale scores in BL-R, which assesses developmental parameters. Although there are no controlled studies assessing the psychomotor development of children with GERD, our findings are consistent with a case report of a child with GERD presenting with a delay in language acquisition (45). Among the subscales, language and socialization had the lowest mean scores; this is consistent with the findings of Machado et al (45), who suggested that there was a relation between feeding and oral language problems. Our findings can be interpreted on the basis of mother–child interactions. Developmental tasks throughout childhood focus on developing a sense of self and acquiring autonomy in all of the areas of life (46). Timing, sensitivity, and interaction patterns with the child are important in the development of self-regulation and a sense of self. The mother of a child with GERD may interfere with this process by overfeeding to compensate for presumed lost food or by limiting food intake to prevent spitting (47). Feeding is a dimension of this interaction and has important biological and psychological functions: it enables the child to grow physically and psychologically. Disturbances in feeding result in undernutrition, which can seriously affect a child's development, behavior, and cognitive skills (48). In general, mother–child interactions are critical to the child's development, especially regarding language. Psychosocial factors such as mother–child interactions, maternal education, and socioeconomic level are related to the cognitive development of toddlers with feeding problems (49).
There are several limitations of the present study. First, because the children were assessed only once, we could not confirm whether a reflux caused by infant distress causes maternal depression or anxiety or whether maternal depression or anxiety causes infant distress, which, in turn, may convert physiological reflux into pathological reflux. Prospective studies with longitudinal designs including cohort groups may reveal an association between depression and anxiety with feeding problems in children with GERD. Insecure attachment may play a role in feeding problems such as forced feeding and FTT because attachment has its origins in maternal infancy.
Second, feeding problems were assessed by maternal interview (by questions in the sociodemographic questionnaire), which depends solely on the subjective ratings of the mother. Maternal eating attitudes may affect the awareness of the mother with respect to feeding, which may lead them to exaggerate their concerns about their child's feeding. Therefore, studies using objective standardized assessments of feeding are needed.
Third, the sample size was relatively small. Although GERD is common in infants and toddlers, we were able to recruit only 39 patients. This is due to the strict exclusion criteria: children with comorbid medical illness (the number of such children was high) were excluded.
A clinical implication of these findings is that children with GERD should be evaluated in terms of feeding behaviors such as food refusal and maternal psychopathology. The aspects of maternal psychopathology that should be evaluated are depression, disturbed eating attitudes, and insecure attachment. The disordered interactions between the mother and child as well as maladaptive feeding behaviors should receive appropriate and prompt intervention before a negative reinforcement to feeding can develop. Such intervention should involve a multidisciplinary approach from clinicians including a pediatric gastroenterologist and child psychiatrist. Developmental assessment should also be kept in mind when evaluating these children.
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