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Parental Bonding and Inflammatory Bowel Disease
Parental Bonding and Inflammatory Bowel Disease Alessandro Agostini, M.D., Fernando Rizzello, M.D. Gianni Ravegnani, M.D., Paolo Gionchetti, M.D. Rosy Tambasco, M.D., Mauro Ercolani, M.D. Massimo Campieri, M.D.
Background: Previous studies have shown a relationship between inflammatory bowel disease (IBD) and psychological stress. Adverse parenting is recognized as an important risk factor for the development of psychiatric disorders in adulthood. Objective: The authors sought to further investigate this relationship by clarifying aspects of the bonding relationship in IBD patients and control subjects. Method: A group of 307 patients with IBD and a group of 307 healthy subjects filled out the questionnaire Parental Bonding Instrument. Results: Patients with IBD perceived their parents’ behaviors as characterized by low care and paternal overprotection; the category Optimal Parenting differs highly in the two samples. Conclusion: This study demonstrated an association between inadequate parenting and a chronic physical illness. These findings are consistent with a growing literature that links early parental experience to chronic illness. (Psychosomatics 2010; 51:14 –21)
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nflammatory bowel disease (IBD) constitutes chronic, idiopathic diseases with a relapsing and remitting course. IBD include both Crohn’s disease (CD) and ulcerative colitis (UC). IBD traditionally has been regarded as a psychosomatic disease,1,2 although recently this view has been criticized and disputed.3 Many studies have shown a high incidence of depression in patients with IBD4,5 and recently Varghese et al.6 have speculated that pre existing mood disorder may facilitate the expression and the course of IBD. On the other hand, other authors have suggested that depression might be secondary to the disability imposed by a chronic disease such as IBD.7,8 Although the impact of life events in the recurrence of Received October 16, 2007; revised December 19, 2007; accepted January 2, 2008. From Univ. of Bologna, Dept. of Psychology, and Dept. of Internal Medicine, Gastroenterology, IBD Unit, Bologna, Italy. Send correspondence and reprint requests to Dr. Alessandro Agostini, Univ. of Bologna, IBD Unit, S. Orsola-Malpighi Hospital, Bologna, Italy. e-mail: [email protected] © 2010 The Academy of Psychosomatic Medicine
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IBD is unclear,9,10 the relationship between psychological stress and IBD has been well established.11–15 Recent findings suggest that stress-induced alterations may be mediated through changes in the hypothalamic–pituitary– adrenal (HPA) axis. Psychological stress stimulates the release of corticotrophin-releasing factor (CRF) from the hypothalamus, causing the secretion of adrenocorticotrophin hormone (ACTH) from the pituitary gland. ACTH, in turn, stimulates the release of cortisol from the adrenal cortex. Furthermore, it is increasingly recognized that cortisol and CRH interact directly with the immune system. Numerous studies demonstrate that maladaptive neuroendocrine responses of the sympathetic nervous system (SNS) to stress can function as risk factors for the initiation and progression of chronic, inflammatory diseases.16 In another recent study, Maudsley et al.17 concluded that, in humans, acute psychological stress can induce systemic and mucosal pro-inflammatory responses. Also, a recent study has shown that, in animal models, chronic psychoPsychosomatics 51:1, January-February 2010
Agostini et al. logical stress alters epithelial-cell turnover and epithelial barrier function in the ileum.18 Likewise, alterations of intestinal permeability have been demonstrated in patients with IBD. Indeed, this alteration is one of the commonly recognized alterations in both patients with Crohn’s disease and their first-degree relatives.19 Furthermore, in an animal model, “depression” caused by neonatal maternal separation is associated with alteration in gut physiology and permeability.6 Inadequate parenting is recognized as a risk factor for the development of psychiatric disorders in adulthood. Indeed, theorists and clinicians from a wide range of disciplinary perspectives defined deficient parenting as an important risk factor for the subsequent occurrence of depression.20 Also, adverse childhood experiences, such as childhood parental loss, are proved to be risk factors even for the development of organic diseases in adulthood; these include ischemic heart disease, obesity, and elevated blood pressure;21 and the linkage between adverse parenting and CRF and cortisol level has been investigated in recent studies.22,23 Infancy, childhood, and adolescence are critical periods, characterized by increased vulnerability to stressors. Exposure of the developing brain to adverse environmental factors such as an inadequate parenting may have effects that last for the entire life of the individual. These effects include disregulation of both the HPA axis and SNS and hyperactivity of the limbic system, with resultant amygdala hyperfunctioning (fear reaction) and decreased activity of the meso-cortico-limbic dopaminergic system (dysthymia, addictive behaviors).24 In the international literature, there are articles that examine attachment in CU,25 but a study of parental bonding and IBD still has not been done. Parenting experiences, particularly lack of care and overprotection, as measured by the Parental Bonding Instrument,26 are associated with an increased risk of a wide variety of forms of psychiatric disorders.20 The PBI is shown to be a stable, reliable, and valid instrument to measure parental behaviors.27 The aim of this study is to evaluate parental bonding in patients with IBD, as compared with healthy subjects. METHOD Design We used a case– control design. The assessment instruments used were administered by specialists from the Department of Psychology of the University of Bologna. Psychosomatics 51:1, January-February 2010
The study was granted ethical approval by the local ethics committee. After being given a full explanation of the study, all participants gave their signed consent. Patient Population We screened a sample of patients with IBD (N⫽800, who were members of the association AMICI Emilia Romagna (Associazione per le Malattie Infiammatorie Croniche Intestinali). AMICI is an association of IBD patients in the region of Emilia Romagna, the capital of which is Bologna. Potential participants were contacted by mail to be included in this study; 354 patients accepted and filled out the questionnaires we mailed; 307 patients (174 CD, 133 UC) were included in the present study. All patients were diagnosed with IBD established by the physicians of the IBD Unit of S. Orsola-Malpighi Hospital in Bologna. The diagnosis of IBD was based on endoscopic, histological, or radiological findings. Inclusion criteria were clinical remission, evaluated by a CD Activity Index (CDAI)28 ⬍150 in patients with CD and a clinical activity index (CAI)29 ⬍2 in patients with UC. Exclusion criteria were the following: current steroid treatment, active disease, and use of antidepressant drugs. Demographic and clinical characteristics of the sample are summarized in Table 1. Control Group The control group was made up of 307 subjects randomly chosen from the general population, living in the TABLE 1.
Demographic and Clinical Characteristics of IBD Patients and Control Subjects IBD Patients Control Group
Characteristic N Age, years, mean Men Women Education Primary school Secondary school High school Degree Unknown Marital status Single Married Divorced Widowed Unknown Pathologies Kind
307 43.14 150 157 21 74 146 61 5 95 186 12 5 9 CD: 174 UC: 133
307 42.69 142 165 17 78 142 65 5 106 174 15 2 10
IBD: inflammatory bowel disease; CD: Crohn’s disease; UC: ulcerative colitis.
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Parental Bonding and IBD same geographic area as the patients’ group. Personnel from the Department of Psychology of University of Bologna requested 800 subjects to participate in the study; 443 subjects agreed to participate. These persons were interviewed to exclude the presence of acute and chronic pathologies. For the purpose of this study, we decided to exclude people with acute or chronic pathologies, intestinal pathologies, or those who were being treated with steroids or antidepressants; 92 subjects were excluded because they did not meet the requirements, and 351 received and completed the questionnaire; 16 participants were excluded because they completed the questionnaire incorrectly. From the remaining 335, 307 were selected to match the sex, age, education, and marital-status frequency distributions of the patients’ population. The demographic characteristics of the sample group are described in Table 1. Assessment The group of healthy subjects and the group of patients with IBD filled out the Parental Bonding Instrument (PBI) questionnaire. The PBI is a self-report questionnaire with 25 items that measure parental styles, recalled by the respondents from the first 16 years of life. The PBI is scored separately for the father and mother so as to evaluate the relationship between the respondents and each of their parents as they subjectively perceived them. The respondents are asked to score their parents’ attitudes or behaviors each separately, using a 4-point Likert scale (“very much like,” “moderately like,” “moderately unlike,” “very unlike”). Two parental styles are measured by the PBI: Care and Overprotection. The child-rearing styles are divided into four categories (PBI quadrants) that are: optimal bonding (high care, low control), neglectful bonding (low care, low control), affectionate constraint (high care, high control), and affectionless control (low care, high control). This last category has been proposed by Parker et al.30 and confirmed by Sato et al.31 as a very maladaptive form of parenting, which results in a particular vulnerability to the occurrence of psychopathology. The category, “affectionless control” reveals that the subjects report the parenting they received as characterized by coldness and rejection (instead of care and warmth) and by over-control and intrusiveness (instead of encouragement to psychological autonomy and exploration of the environment). The psychometric properties of this instrument are good: it is a very easy-to-use tool for researchers; it has 16
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long-term stability;24 and its subscales have a high level of test–retest reliability and internal consistency.26,32,33 In this study, we used the cutoff points suggested by the Black Dog Institute of Sydney, Australia. The Italian version used in this study is the one provided by Poerio34 and authorized for research purposes.35 The group of patients with IBD also filled out the Symptoms Checklist questionnaire (SCL-90 –R).36 The SCL-90 –R is a self-evaluation questionnaire with 90 items. This instrument is widely used by researchers and clinicians because it leads to an evaluation of a wide variety of forms of psychiatric symptoms. In this way, researchers can obtain a general valuation of psychological suffering of the patients. Psychological discomfort is evaluated on nine primary dimensions: somatization (S), obsessive-compulsive symptoms (OCD), interpersonal sensitivity (IS), depression (D), anxiety (A), anger/hostility (H), phobic anxiety (Ph A), paranoid ideation (IP), and psychoticism (P). The subjects must describe how much they have suffered from a symptom in the past month. Each of the 90 items is rated on a 5-point Likert scale of distress, ranging from “not at all: 0” to “extremely: 4.” The responses are subsequently combined in the nine primary symptom dimensions described above. Also, three global indices provide measures of overall psychological distress. These are: the Global Severity Index (GSI), the Positive Symptom Total (PST), and the Positive Symptom Distress Index (PSDI). Descriptive results are reported as T scores (normative mean score: 50; standard deviation [SD]: 10). Clinically important distress corresponds to T-scores ⱖ63 (ⱖ91st percentile). Statistical Analysis The statistical analysis was done with SPSS for Windows (SPSS; Chicago, IL). Results are expressed as means (SD). Comparison of differences between groups was performed by Student’s t-test for continuous variables and the chi-square test for dichotomous variables. Correlation coefficients were calculated to test for associations between care and overprotection and the scores obtained by SCL90 –R in patients with IBD. For statistical analyses, we used raw scores on the SCL-90 –R. Correlation coefficients were calculated with Pearson r. RESULTS There were no significant differences between the groups on demographic characteristics, and no significant differPsychosomatics 51:1, January-February 2010
Agostini et al. ences were found in PBI and SCL-90 –R scores between patients with CD and those with UC. Table 2 presents the mean scores of the two groups on the PBI and the results of the t-test used to compare the groups. In three dimensions, there was a p level ⬍0.05. On the Care scale, both fathers (p⫽0.044) and mothers (p⫽0.013) of patients with IBD were perceived as less caring than those of healthy group. On the Overprotection scale, rather, only the fathers of patients with IBD were perceived as more overprotective (p⫽0.028) than those of the healthy group. There were no significant differences in the dimension of maternal overprotection. Table 3 shows the number of patients with IBD and healthy subjects in each of the four categories. For maternal styles only “affectionate constraint” showed no significant differences. Patients who received “affectionless control” (of 307, 116 Patients versus 100 Controls) and “neglectful parenting” (of 307, 73 Patients versus 52 Controls) were significantly more numerous (p ⬍0.05) than those in the healthy sample (Controls). Moreover, of 307 subjects, those Patients who perceived optimal parenting from the mother were significantly fewer (p ⬍0.001) than healthy ones: 74 versus 121. Similarly, with regard to paternal styles, of 307 subjects, 72 patients with IBD versus 115 healthy subjects perceived optimal parenting (p ⬍0.001), and 93 Patients versus 67 Controls perceived neglectful parenting (p ⬍0.01). Table 4 presents the T-scores for the SCL-90 –R subscales. The table shows the number and the percentage of patients with IBD who are in the clinical range (T score ⱖ63); 32 patients of 307 (10.42%) were considered psychologically distressed. Indeed, 50 patients had clinically important scores on the GSI. Using the Pearson r, correlation analyses were undertaken between the four dimensions of PBI and the nine dimensions described by the SCL-90 –R. The Care factor of the PBI, both maternal and pater-
TABLE 2.
PBI Scores in IBD Patients and Control Subjects IBD Patients Control Subjects (Nⴝ307) (Nⴝ307)
Care: Mother Overprotection: Mother Care: Father Overprotection: Father
23.60 (8.30) 14.81 (7.16) 21.10 (8.56) 13.15 (8.18)
25.15 (7.16) 14.03 (8.57) 22.44 (7.78) 11.76 (7.38)
t 2.49* –1.16 2.02* –2.21*
Values are mean (standard deviation). PBI: Parental Bonding Instrument; IBD: inflammatory bowel disease. *p ⬍0.05.
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TABLE 3.
PBI Categories in IBD Patients and Control Subjects
Mother
IBD Patients
Control Subjects
2
Affectionate constraint Affectionless control Neglectful parenting Optimal parenting
44 116 73 74
34 100 52 121
0.45 6.12* 6.71* 24.70***
Father
IBD Patients
Control Subjects
2
Affectionate constraint Affectionless control Neglectful parenting Optimal parenting
33 109 93 72
25 100 67 115
0.73 1.93 8.87** 20.91***
PBI: Parental Bonding Instrument; IBD: inflammatory bowel disease. *p ⬍0.05; **p ⬍0.01; ***p ⬍0.001.
TABLE 4.
SCL-90 –R Subscales in 307 IBD Patients: N (%) of Patients With Clinically-Important Scores N (%)
Somatization Obsessive-Compulsive symptoms Interpersonal Sensitivity Depression Anxiety Anger/Hostility Phobic Anxiety Paranoid Ideation Psychoticism Global Severity Index (GSI)
29 (9.45) 30 (9.77) 38 (12.38) 39 (12.70) 31 (10.09) 33 (10.75) 26 (8.47) 33 (10.75 27 (8.79) 32 (10.42)
SCL: Symptom Checklist.
nal, was correlated with all the dimensions of the SCL90 –R. A high correlation was found between parental low Care and any of the psychological distress measures. Similarly, the other PBI subscale (Overprotection) was strongly correlated with all the symptoms of psychological suffering. The strongest correlations were found between the symptoms of psychological distress and overprotection. Indeed, every Pearson correlation coefficient reached a significance level of p ⬍0.001. Correlation coefficients are presented in Table 5.
DISCUSSION The data presented show that, as compared with healthy subjects, the parental bonding perceived by patients with IBD is different. Patients with IBD perceived their parhttp://psy.psychiatryonline.org
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Parental Bonding and IBD
TABLE 5.
Pearson Correlations (r) Between PBI and SCL-90 –R Scores in IBD Patients Care: Mother
Overprotection: Mother
Care: Father
Overprotection: Father
–0.172** –0.217*** –0.181** –0.248*** –0.255*** –0.117* –0.164** –0.182** –0.134* –0.225***
0.204*** 0.283*** 0.266*** 0.284*** 0.284*** 0.191*** 0.197*** 0.276*** 0.234*** 0.295***
–0.171** –0.213*** –0.243*** –0.170** –0.195*** –0.174** –0.124* –0.233*** –0.175** –0.215***
0.236*** 0.282*** 0.292*** 0.253*** 0.289*** 0.264*** 0.238*** 0.357*** 0.223*** 0.320***
Somatization Obsessive-Compulsive Disorder Interpersonal Sensitivity Depression Anxiety Anger/Hostility Phobic Anxiety Paranoid Ideation Psychoticism Global Severity Index
PBI: Parental Bonding Index; SCL-90 –R: Symptom Checklist, 90-item, Revised. *p ⬍0.05; **p ⬍0.01; ***p ⬍0.001.
ents’ behaviors as characterized by low care and high paternal protection. Even the analysis of the four PBI categories shows that optimal parenting differs highly between the two samples. To summarize, we can affirm that patients with IBD described difficulties of warmth, understanding, independence, and developing autonomy in relationships with parents. On the basis of the present findings, it could be argued that perceived parental bonding, observed in patients with IBD, can be regarded as inadequate parenting. Inadequate early caregiving has been described in several mental illnesses: in anorexia and bulimia patients,37 in panic disorders,38 in schizophrenia,39 and in drug-dependent patients.40 Furthermore, many authors demonstrated that lack of parental care from the father and the mother is related to increased lifetime susceptibility to depression.20,41–43 In contrast with earlier studies, this research has demonstrated an association between adverse parenting and a chronic, physical illness. Given this link, we may debate whether inadequate parenting is a risk factor for developing this chronic, inflammatory pathology. We can consider two different hypotheses: The first is that it is the individual’s perception of inadequate parenting that leads to the greatest risk for subsequent psychological distress correlated with the clinical history and symptoms in IBD. Second, it could be hypothesized that the presence of IBD can alter and worsen the perception of patients’ own parenting. Those hypotheses should be regarded in light of some limitations. The first limitation is that PBI is an instrument designed to measure retrospectively-recalled parents’ behaviors and attitudes. Therefore, there is the possibility that recall biases or current mood state could influence the 18
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results. For example, the indicators of psychological distress revealed by the SCL-90 –R questionnaire answered by patients can influence the subjects’ memories of the relationships within the family negatively. Second, we have to consider the so called “search for meaning” hypothesis. Not surprisingly, a search for meaning by patients with IBD could lead to biased responses to the PBI questionnaire. The etiology of IBD is still unknown, and, not unusually, patients affected may reject the idea that there is no clear cause or scientific reason for their disease. This factor could influence recall, eliciting a memory of lower level of care or higher level of overprotection. The effect of the “search for meaning” has been described and evaluated even in patients with mental illness.44 The third limit of this study could be a major predisposition of patients with adverse parental experiences to participate in research that explores those factors. In the present study, 307 patients, among a group of 800, responded and participated in the research. A larger sample could probably reduce this bias. On the other hand, long-term reliability for the PBI has been proven in several studies.26,27,32,33 Also, Wilhelm et al.27 demonstrated the stability of the PBI over a 20-year period and suggested that recollections of one’s parental environment are not substantially influenced by gender and history of life experiences. Even the influence of important factors such as mood state is limited,33,45,46 and subjects’ perceptions seem not to be shifted with fluctuations in depressed mood.27 Also, the effect of the “search for meaning” should not be over-emphasized. In patients with chronic pain, for instance, the PBI results are not substantially affected by this factor.47 To summarize, bearing in mind all these factors, we are inclined to believe that Psychosomatics 51:1, January-February 2010
Agostini et al. life experiences, such as the onset of IBD, should have no determining effect on the perception of parental bonding. Given the validity of adult retrospective-recall of adverse childhood experiences,48 we can suggest that adverse parenting may play a role in the clinical history of patients with IBD. We can also speculate that these experiences can be considered risk factors for the subsequent onset of IBD. This study is preliminary, and its design is not able to clarify whether the association we found between adverse parenting and IBD can be evaluated as a causal link. Actually, in international literature, there is not sufficient evidence to suggest that psychological stress can enhance IBD. Instead, recent findings illustrate that acute psychological stress and depression can influence gut physiology in humans17 and worsen a pre-existing IBD in animal models. Indeed, the recent study of Varghese et al.,6 which focused on maternally-deprived mice, could reinforce the hypothesis of this association. An acute colitis condition was induced in both maternally-separated and non-separated adult mice by dextran sulfate sodium (DSS) in drinking water. After DSS administration, adult maternallyseparated animals showed a more severe colitis, greater weight loss, greater clinical disease scores, greater microscopic damage, and a greater infiltration by inflammatory cells than those of non-separated animals. Of course, the acute colitis in mice was artificially induced, and the animal model is different from humans. Yet the findings of this study have prompted suggestions that, even in humans, adverse parenting, characterized by low care, could play an important role in the clinical history of IBD. There is growing evidence that adverse childhood experiences lead to disregulation of the HPA axis and can have effect on cortisol responses to stress in adulthood. In other words, HPAaxis disregulation may play an important role in the pathway leading from disturbance in early parental experiences to adult disorders.23 It is possible that CRF released in response to stressful stimuli activates mast cells in the gut. The release of mast-cell mediators may increase bacterial adherence and uptake. This, in turn, could lead to the sensitization of T-cells and the production of tumor necrosis factor ␣ (TNF-␣). TNF-␣ is a key cytokine for the inflammatory cascade in IBD and may both initiate inflammation and cause a secondary increase in gut permeability. Furthermore, CRF also appears to have a secondary peripheral action as an inflammatory cytokine.13 In the present study, we examined the association Psychosomatics 51:1, January-February 2010
between recalled parental bonding experiences and a range of common mental disorders. First, we could establish a strong association between low maternal care and many forms of adult psychopathology. As suggested in a recent study,20 lack of maternal care is correlated in a nonspecific manner with a wide variety of forms of adult psychopathology, and not only to depression, as initially proposed by Parker.30 Second, we observed a strong association between paternal care and symptoms of psychological distress. Heider et al.,42 in fact, found no difference between the effects of care of the mother and the care of the father in the occurrence of mood disorders. Third, in patients with IBD, the dimension of overprotection, surprisingly, showed the strongest association with symptoms of mental disorders. This finding differs from those reported by Enns et al.20 and Heider et al.42 In our opinion, this study advances our understanding of a specific psychological factor that may contribute to current psychological distress in patients with IBD. Usually, the literature discusses psychological stress in a nonspecific way. This study attempts to understand the contents and study the specific factors of stress. In conclusion, the present study enhances the belief in a link between the parent– child bond and the development of physical illness in adulthood. In patients with IBD, we could speculate that adverse parenting is causally linked with psychological distress developed in adulthood, and, moreover, this finding could be correlated with the alterations in gut physiology and permeability proved in the animal model6 and also in humans.17 The neuroendocrine changes induced by stress during childhood involving the HPA axis and the limbic system may represent the link between inflammatory disease and psychological distress in adulthood. Similar considerations are also reported by researchers investigating the link between early parenting and hypertension.49,50 The recent study by Maunder et al.25 focused on attachment, and CU confirms the researchers’ interest in these arguments. Further studies could corroborate our hypothesis and establish a causal link between attachment and early parental experiences and the onset and clinical course of IBD. The authors are grateful to the volunteers of Association Amici Emilia Romagna and to the association’s directors. This study was supported by Fondazione Cassa di Risparmio in Bologna. http://psy.psychiatryonline.org
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Background: Previous studies have shown a relationship between inflammatory bowel disease (IBD) and psychological stress. Adverse parenting is recognized as an important risk factor for the development of psychiatric disorders in adulthood. Objective: The authors sought to further investigate this relationship by clarifying aspects of the bonding relationship in IBD patients and control subjects. Method: A group of 307 patients with IBD and a group of 307 healthy subjects filled out the questionnaire Parental Bonding Instrument. Results: Patients with IBD perceived their parents’ behaviors as characterized by low care and paternal overprotection; the category Optimal Parenting differs highly in the two samples. Conclusion: This study demonstrated an association between inadequate parenting and a chronic physical illness. These findings are consistent with a growing literature that links early parental experience to chronic illness. (Psychosomatics 2010; 51:14 –21)
I
nflammatory bowel disease (IBD) constitutes chronic, idiopathic diseases with a relapsing and remitting course. IBD include both Crohn’s disease (CD) and ulcerative colitis (UC). IBD traditionally has been regarded as a psychosomatic disease,1,2 although recently this view has been criticized and disputed.3 Many studies have shown a high incidence of depression in patients with IBD4,5 and recently Varghese et al.6 have speculated that pre existing mood disorder may facilitate the expression and the course of IBD. On the other hand, other authors have suggested that depression might be secondary to the disability imposed by a chronic disease such as IBD.7,8 Although the impact of life events in the recurrence of Received October 16, 2007; revised December 19, 2007; accepted January 2, 2008. From Univ. of Bologna, Dept. of Psychology, and Dept. of Internal Medicine, Gastroenterology, IBD Unit, Bologna, Italy. Send correspondence and reprint requests to Dr. Alessandro Agostini, Univ. of Bologna, IBD Unit, S. Orsola-Malpighi Hospital, Bologna, Italy. e-mail: [email protected] © 2010 The Academy of Psychosomatic Medicine
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IBD is unclear,9,10 the relationship between psychological stress and IBD has been well established.11–15 Recent findings suggest that stress-induced alterations may be mediated through changes in the hypothalamic–pituitary– adrenal (HPA) axis. Psychological stress stimulates the release of corticotrophin-releasing factor (CRF) from the hypothalamus, causing the secretion of adrenocorticotrophin hormone (ACTH) from the pituitary gland. ACTH, in turn, stimulates the release of cortisol from the adrenal cortex. Furthermore, it is increasingly recognized that cortisol and CRH interact directly with the immune system. Numerous studies demonstrate that maladaptive neuroendocrine responses of the sympathetic nervous system (SNS) to stress can function as risk factors for the initiation and progression of chronic, inflammatory diseases.16 In another recent study, Maudsley et al.17 concluded that, in humans, acute psychological stress can induce systemic and mucosal pro-inflammatory responses. Also, a recent study has shown that, in animal models, chronic psychoPsychosomatics 51:1, January-February 2010
Agostini et al. logical stress alters epithelial-cell turnover and epithelial barrier function in the ileum.18 Likewise, alterations of intestinal permeability have been demonstrated in patients with IBD. Indeed, this alteration is one of the commonly recognized alterations in both patients with Crohn’s disease and their first-degree relatives.19 Furthermore, in an animal model, “depression” caused by neonatal maternal separation is associated with alteration in gut physiology and permeability.6 Inadequate parenting is recognized as a risk factor for the development of psychiatric disorders in adulthood. Indeed, theorists and clinicians from a wide range of disciplinary perspectives defined deficient parenting as an important risk factor for the subsequent occurrence of depression.20 Also, adverse childhood experiences, such as childhood parental loss, are proved to be risk factors even for the development of organic diseases in adulthood; these include ischemic heart disease, obesity, and elevated blood pressure;21 and the linkage between adverse parenting and CRF and cortisol level has been investigated in recent studies.22,23 Infancy, childhood, and adolescence are critical periods, characterized by increased vulnerability to stressors. Exposure of the developing brain to adverse environmental factors such as an inadequate parenting may have effects that last for the entire life of the individual. These effects include disregulation of both the HPA axis and SNS and hyperactivity of the limbic system, with resultant amygdala hyperfunctioning (fear reaction) and decreased activity of the meso-cortico-limbic dopaminergic system (dysthymia, addictive behaviors).24 In the international literature, there are articles that examine attachment in CU,25 but a study of parental bonding and IBD still has not been done. Parenting experiences, particularly lack of care and overprotection, as measured by the Parental Bonding Instrument,26 are associated with an increased risk of a wide variety of forms of psychiatric disorders.20 The PBI is shown to be a stable, reliable, and valid instrument to measure parental behaviors.27 The aim of this study is to evaluate parental bonding in patients with IBD, as compared with healthy subjects. METHOD Design We used a case– control design. The assessment instruments used were administered by specialists from the Department of Psychology of the University of Bologna. Psychosomatics 51:1, January-February 2010
The study was granted ethical approval by the local ethics committee. After being given a full explanation of the study, all participants gave their signed consent. Patient Population We screened a sample of patients with IBD (N⫽800, who were members of the association AMICI Emilia Romagna (Associazione per le Malattie Infiammatorie Croniche Intestinali). AMICI is an association of IBD patients in the region of Emilia Romagna, the capital of which is Bologna. Potential participants were contacted by mail to be included in this study; 354 patients accepted and filled out the questionnaires we mailed; 307 patients (174 CD, 133 UC) were included in the present study. All patients were diagnosed with IBD established by the physicians of the IBD Unit of S. Orsola-Malpighi Hospital in Bologna. The diagnosis of IBD was based on endoscopic, histological, or radiological findings. Inclusion criteria were clinical remission, evaluated by a CD Activity Index (CDAI)28 ⬍150 in patients with CD and a clinical activity index (CAI)29 ⬍2 in patients with UC. Exclusion criteria were the following: current steroid treatment, active disease, and use of antidepressant drugs. Demographic and clinical characteristics of the sample are summarized in Table 1. Control Group The control group was made up of 307 subjects randomly chosen from the general population, living in the TABLE 1.
Demographic and Clinical Characteristics of IBD Patients and Control Subjects IBD Patients Control Group
Characteristic N Age, years, mean Men Women Education Primary school Secondary school High school Degree Unknown Marital status Single Married Divorced Widowed Unknown Pathologies Kind
307 43.14 150 157 21 74 146 61 5 95 186 12 5 9 CD: 174 UC: 133
307 42.69 142 165 17 78 142 65 5 106 174 15 2 10
IBD: inflammatory bowel disease; CD: Crohn’s disease; UC: ulcerative colitis.
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Parental Bonding and IBD same geographic area as the patients’ group. Personnel from the Department of Psychology of University of Bologna requested 800 subjects to participate in the study; 443 subjects agreed to participate. These persons were interviewed to exclude the presence of acute and chronic pathologies. For the purpose of this study, we decided to exclude people with acute or chronic pathologies, intestinal pathologies, or those who were being treated with steroids or antidepressants; 92 subjects were excluded because they did not meet the requirements, and 351 received and completed the questionnaire; 16 participants were excluded because they completed the questionnaire incorrectly. From the remaining 335, 307 were selected to match the sex, age, education, and marital-status frequency distributions of the patients’ population. The demographic characteristics of the sample group are described in Table 1. Assessment The group of healthy subjects and the group of patients with IBD filled out the Parental Bonding Instrument (PBI) questionnaire. The PBI is a self-report questionnaire with 25 items that measure parental styles, recalled by the respondents from the first 16 years of life. The PBI is scored separately for the father and mother so as to evaluate the relationship between the respondents and each of their parents as they subjectively perceived them. The respondents are asked to score their parents’ attitudes or behaviors each separately, using a 4-point Likert scale (“very much like,” “moderately like,” “moderately unlike,” “very unlike”). Two parental styles are measured by the PBI: Care and Overprotection. The child-rearing styles are divided into four categories (PBI quadrants) that are: optimal bonding (high care, low control), neglectful bonding (low care, low control), affectionate constraint (high care, high control), and affectionless control (low care, high control). This last category has been proposed by Parker et al.30 and confirmed by Sato et al.31 as a very maladaptive form of parenting, which results in a particular vulnerability to the occurrence of psychopathology. The category, “affectionless control” reveals that the subjects report the parenting they received as characterized by coldness and rejection (instead of care and warmth) and by over-control and intrusiveness (instead of encouragement to psychological autonomy and exploration of the environment). The psychometric properties of this instrument are good: it is a very easy-to-use tool for researchers; it has 16
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long-term stability;24 and its subscales have a high level of test–retest reliability and internal consistency.26,32,33 In this study, we used the cutoff points suggested by the Black Dog Institute of Sydney, Australia. The Italian version used in this study is the one provided by Poerio34 and authorized for research purposes.35 The group of patients with IBD also filled out the Symptoms Checklist questionnaire (SCL-90 –R).36 The SCL-90 –R is a self-evaluation questionnaire with 90 items. This instrument is widely used by researchers and clinicians because it leads to an evaluation of a wide variety of forms of psychiatric symptoms. In this way, researchers can obtain a general valuation of psychological suffering of the patients. Psychological discomfort is evaluated on nine primary dimensions: somatization (S), obsessive-compulsive symptoms (OCD), interpersonal sensitivity (IS), depression (D), anxiety (A), anger/hostility (H), phobic anxiety (Ph A), paranoid ideation (IP), and psychoticism (P). The subjects must describe how much they have suffered from a symptom in the past month. Each of the 90 items is rated on a 5-point Likert scale of distress, ranging from “not at all: 0” to “extremely: 4.” The responses are subsequently combined in the nine primary symptom dimensions described above. Also, three global indices provide measures of overall psychological distress. These are: the Global Severity Index (GSI), the Positive Symptom Total (PST), and the Positive Symptom Distress Index (PSDI). Descriptive results are reported as T scores (normative mean score: 50; standard deviation [SD]: 10). Clinically important distress corresponds to T-scores ⱖ63 (ⱖ91st percentile). Statistical Analysis The statistical analysis was done with SPSS for Windows (SPSS; Chicago, IL). Results are expressed as means (SD). Comparison of differences between groups was performed by Student’s t-test for continuous variables and the chi-square test for dichotomous variables. Correlation coefficients were calculated to test for associations between care and overprotection and the scores obtained by SCL90 –R in patients with IBD. For statistical analyses, we used raw scores on the SCL-90 –R. Correlation coefficients were calculated with Pearson r. RESULTS There were no significant differences between the groups on demographic characteristics, and no significant differPsychosomatics 51:1, January-February 2010
Agostini et al. ences were found in PBI and SCL-90 –R scores between patients with CD and those with UC. Table 2 presents the mean scores of the two groups on the PBI and the results of the t-test used to compare the groups. In three dimensions, there was a p level ⬍0.05. On the Care scale, both fathers (p⫽0.044) and mothers (p⫽0.013) of patients with IBD were perceived as less caring than those of healthy group. On the Overprotection scale, rather, only the fathers of patients with IBD were perceived as more overprotective (p⫽0.028) than those of the healthy group. There were no significant differences in the dimension of maternal overprotection. Table 3 shows the number of patients with IBD and healthy subjects in each of the four categories. For maternal styles only “affectionate constraint” showed no significant differences. Patients who received “affectionless control” (of 307, 116 Patients versus 100 Controls) and “neglectful parenting” (of 307, 73 Patients versus 52 Controls) were significantly more numerous (p ⬍0.05) than those in the healthy sample (Controls). Moreover, of 307 subjects, those Patients who perceived optimal parenting from the mother were significantly fewer (p ⬍0.001) than healthy ones: 74 versus 121. Similarly, with regard to paternal styles, of 307 subjects, 72 patients with IBD versus 115 healthy subjects perceived optimal parenting (p ⬍0.001), and 93 Patients versus 67 Controls perceived neglectful parenting (p ⬍0.01). Table 4 presents the T-scores for the SCL-90 –R subscales. The table shows the number and the percentage of patients with IBD who are in the clinical range (T score ⱖ63); 32 patients of 307 (10.42%) were considered psychologically distressed. Indeed, 50 patients had clinically important scores on the GSI. Using the Pearson r, correlation analyses were undertaken between the four dimensions of PBI and the nine dimensions described by the SCL-90 –R. The Care factor of the PBI, both maternal and pater-
TABLE 2.
PBI Scores in IBD Patients and Control Subjects IBD Patients Control Subjects (Nⴝ307) (Nⴝ307)
Care: Mother Overprotection: Mother Care: Father Overprotection: Father
23.60 (8.30) 14.81 (7.16) 21.10 (8.56) 13.15 (8.18)
25.15 (7.16) 14.03 (8.57) 22.44 (7.78) 11.76 (7.38)
t 2.49* –1.16 2.02* –2.21*
Values are mean (standard deviation). PBI: Parental Bonding Instrument; IBD: inflammatory bowel disease. *p ⬍0.05.
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TABLE 3.
PBI Categories in IBD Patients and Control Subjects
Mother
IBD Patients
Control Subjects
2
Affectionate constraint Affectionless control Neglectful parenting Optimal parenting
44 116 73 74
34 100 52 121
0.45 6.12* 6.71* 24.70***
Father
IBD Patients
Control Subjects
2
Affectionate constraint Affectionless control Neglectful parenting Optimal parenting
33 109 93 72
25 100 67 115
0.73 1.93 8.87** 20.91***
PBI: Parental Bonding Instrument; IBD: inflammatory bowel disease. *p ⬍0.05; **p ⬍0.01; ***p ⬍0.001.
TABLE 4.
SCL-90 –R Subscales in 307 IBD Patients: N (%) of Patients With Clinically-Important Scores N (%)
Somatization Obsessive-Compulsive symptoms Interpersonal Sensitivity Depression Anxiety Anger/Hostility Phobic Anxiety Paranoid Ideation Psychoticism Global Severity Index (GSI)
29 (9.45) 30 (9.77) 38 (12.38) 39 (12.70) 31 (10.09) 33 (10.75) 26 (8.47) 33 (10.75 27 (8.79) 32 (10.42)
SCL: Symptom Checklist.
nal, was correlated with all the dimensions of the SCL90 –R. A high correlation was found between parental low Care and any of the psychological distress measures. Similarly, the other PBI subscale (Overprotection) was strongly correlated with all the symptoms of psychological suffering. The strongest correlations were found between the symptoms of psychological distress and overprotection. Indeed, every Pearson correlation coefficient reached a significance level of p ⬍0.001. Correlation coefficients are presented in Table 5.
DISCUSSION The data presented show that, as compared with healthy subjects, the parental bonding perceived by patients with IBD is different. Patients with IBD perceived their parhttp://psy.psychiatryonline.org
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TABLE 5.
Pearson Correlations (r) Between PBI and SCL-90 –R Scores in IBD Patients Care: Mother
Overprotection: Mother
Care: Father
Overprotection: Father
–0.172** –0.217*** –0.181** –0.248*** –0.255*** –0.117* –0.164** –0.182** –0.134* –0.225***
0.204*** 0.283*** 0.266*** 0.284*** 0.284*** 0.191*** 0.197*** 0.276*** 0.234*** 0.295***
–0.171** –0.213*** –0.243*** –0.170** –0.195*** –0.174** –0.124* –0.233*** –0.175** –0.215***
0.236*** 0.282*** 0.292*** 0.253*** 0.289*** 0.264*** 0.238*** 0.357*** 0.223*** 0.320***
Somatization Obsessive-Compulsive Disorder Interpersonal Sensitivity Depression Anxiety Anger/Hostility Phobic Anxiety Paranoid Ideation Psychoticism Global Severity Index
PBI: Parental Bonding Index; SCL-90 –R: Symptom Checklist, 90-item, Revised. *p ⬍0.05; **p ⬍0.01; ***p ⬍0.001.
ents’ behaviors as characterized by low care and high paternal protection. Even the analysis of the four PBI categories shows that optimal parenting differs highly between the two samples. To summarize, we can affirm that patients with IBD described difficulties of warmth, understanding, independence, and developing autonomy in relationships with parents. On the basis of the present findings, it could be argued that perceived parental bonding, observed in patients with IBD, can be regarded as inadequate parenting. Inadequate early caregiving has been described in several mental illnesses: in anorexia and bulimia patients,37 in panic disorders,38 in schizophrenia,39 and in drug-dependent patients.40 Furthermore, many authors demonstrated that lack of parental care from the father and the mother is related to increased lifetime susceptibility to depression.20,41–43 In contrast with earlier studies, this research has demonstrated an association between adverse parenting and a chronic, physical illness. Given this link, we may debate whether inadequate parenting is a risk factor for developing this chronic, inflammatory pathology. We can consider two different hypotheses: The first is that it is the individual’s perception of inadequate parenting that leads to the greatest risk for subsequent psychological distress correlated with the clinical history and symptoms in IBD. Second, it could be hypothesized that the presence of IBD can alter and worsen the perception of patients’ own parenting. Those hypotheses should be regarded in light of some limitations. The first limitation is that PBI is an instrument designed to measure retrospectively-recalled parents’ behaviors and attitudes. Therefore, there is the possibility that recall biases or current mood state could influence the 18
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results. For example, the indicators of psychological distress revealed by the SCL-90 –R questionnaire answered by patients can influence the subjects’ memories of the relationships within the family negatively. Second, we have to consider the so called “search for meaning” hypothesis. Not surprisingly, a search for meaning by patients with IBD could lead to biased responses to the PBI questionnaire. The etiology of IBD is still unknown, and, not unusually, patients affected may reject the idea that there is no clear cause or scientific reason for their disease. This factor could influence recall, eliciting a memory of lower level of care or higher level of overprotection. The effect of the “search for meaning” has been described and evaluated even in patients with mental illness.44 The third limit of this study could be a major predisposition of patients with adverse parental experiences to participate in research that explores those factors. In the present study, 307 patients, among a group of 800, responded and participated in the research. A larger sample could probably reduce this bias. On the other hand, long-term reliability for the PBI has been proven in several studies.26,27,32,33 Also, Wilhelm et al.27 demonstrated the stability of the PBI over a 20-year period and suggested that recollections of one’s parental environment are not substantially influenced by gender and history of life experiences. Even the influence of important factors such as mood state is limited,33,45,46 and subjects’ perceptions seem not to be shifted with fluctuations in depressed mood.27 Also, the effect of the “search for meaning” should not be over-emphasized. In patients with chronic pain, for instance, the PBI results are not substantially affected by this factor.47 To summarize, bearing in mind all these factors, we are inclined to believe that Psychosomatics 51:1, January-February 2010
Agostini et al. life experiences, such as the onset of IBD, should have no determining effect on the perception of parental bonding. Given the validity of adult retrospective-recall of adverse childhood experiences,48 we can suggest that adverse parenting may play a role in the clinical history of patients with IBD. We can also speculate that these experiences can be considered risk factors for the subsequent onset of IBD. This study is preliminary, and its design is not able to clarify whether the association we found between adverse parenting and IBD can be evaluated as a causal link. Actually, in international literature, there is not sufficient evidence to suggest that psychological stress can enhance IBD. Instead, recent findings illustrate that acute psychological stress and depression can influence gut physiology in humans17 and worsen a pre-existing IBD in animal models. Indeed, the recent study of Varghese et al.,6 which focused on maternally-deprived mice, could reinforce the hypothesis of this association. An acute colitis condition was induced in both maternally-separated and non-separated adult mice by dextran sulfate sodium (DSS) in drinking water. After DSS administration, adult maternallyseparated animals showed a more severe colitis, greater weight loss, greater clinical disease scores, greater microscopic damage, and a greater infiltration by inflammatory cells than those of non-separated animals. Of course, the acute colitis in mice was artificially induced, and the animal model is different from humans. Yet the findings of this study have prompted suggestions that, even in humans, adverse parenting, characterized by low care, could play an important role in the clinical history of IBD. There is growing evidence that adverse childhood experiences lead to disregulation of the HPA axis and can have effect on cortisol responses to stress in adulthood. In other words, HPAaxis disregulation may play an important role in the pathway leading from disturbance in early parental experiences to adult disorders.23 It is possible that CRF released in response to stressful stimuli activates mast cells in the gut. The release of mast-cell mediators may increase bacterial adherence and uptake. This, in turn, could lead to the sensitization of T-cells and the production of tumor necrosis factor ␣ (TNF-␣). TNF-␣ is a key cytokine for the inflammatory cascade in IBD and may both initiate inflammation and cause a secondary increase in gut permeability. Furthermore, CRF also appears to have a secondary peripheral action as an inflammatory cytokine.13 In the present study, we examined the association Psychosomatics 51:1, January-February 2010
between recalled parental bonding experiences and a range of common mental disorders. First, we could establish a strong association between low maternal care and many forms of adult psychopathology. As suggested in a recent study,20 lack of maternal care is correlated in a nonspecific manner with a wide variety of forms of adult psychopathology, and not only to depression, as initially proposed by Parker.30 Second, we observed a strong association between paternal care and symptoms of psychological distress. Heider et al.,42 in fact, found no difference between the effects of care of the mother and the care of the father in the occurrence of mood disorders. Third, in patients with IBD, the dimension of overprotection, surprisingly, showed the strongest association with symptoms of mental disorders. This finding differs from those reported by Enns et al.20 and Heider et al.42 In our opinion, this study advances our understanding of a specific psychological factor that may contribute to current psychological distress in patients with IBD. Usually, the literature discusses psychological stress in a nonspecific way. This study attempts to understand the contents and study the specific factors of stress. In conclusion, the present study enhances the belief in a link between the parent– child bond and the development of physical illness in adulthood. In patients with IBD, we could speculate that adverse parenting is causally linked with psychological distress developed in adulthood, and, moreover, this finding could be correlated with the alterations in gut physiology and permeability proved in the animal model6 and also in humans.17 The neuroendocrine changes induced by stress during childhood involving the HPA axis and the limbic system may represent the link between inflammatory disease and psychological distress in adulthood. Similar considerations are also reported by researchers investigating the link between early parenting and hypertension.49,50 The recent study by Maunder et al.25 focused on attachment, and CU confirms the researchers’ interest in these arguments. Further studies could corroborate our hypothesis and establish a causal link between attachment and early parental experiences and the onset and clinical course of IBD. The authors are grateful to the volunteers of Association Amici Emilia Romagna and to the association’s directors. This study was supported by Fondazione Cassa di Risparmio in Bologna. http://psy.psychiatryonline.org
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