European Journal of Obstetrics & Gynecology and Reproductive Biology 174 (2014) 70–75
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European Journal of Obstetrics & Gynecology and Reproductive Biology journal homepage: www.elsevier.com/locate/ejogrb
Maternal–fetal attachment and prenatal diagnosis of heart disease Patricia Ruschel *, Paulo Zielinsky, Cristiane Grings, Julia Pimentel, Liege Azevedo, Rafaele Paniagua, Luiz H. Nicoloso Fetal Cardiology Unit, Instituto de Cardiologia do Rio Grande do Sul/Fundac¸a˜o Universita´ria de Cardiologia, Porto Alegre, Brazil
A R T I C L E I N F O
A B S T R A C T
Article history: Received 13 May 2013 Received in revised form 9 November 2013 Accepted 25 November 2013
Objective: To test the hypothesis that there are differences in the level of maternal–fetal attachment before and after fetal echocardiography in the presence or absence of cardiac abnormalities. Study design: Cohort study in which the mothers responded to a validated Maternal–Fetal Attachment Scale. The study compared a group of pregnant women with diagnosis of fetal heart disease (FHD) with a group without this diagnosis (‘‘no fetal heart disease’’ – NFHD). Results: 197 pregnant women were included, 96 FHD and 101 NFHD. Maternal–fetal attachment at the initial and final periods showed no significant baseline differences between groups (p = 0.081). At the final period, migration from medium to high level of attachment was significantly higher in FHD (p = 0.017). Transition from medium to high levels comparing the initial and final periods was more pronounced in FHD (p = 0.009). Conclusion: Diagnosis of fetal heart disease increases the level of maternal–fetal attachment. ß 2013 Elsevier Ireland Ltd. All rights reserved.
Keywords: Fetal echocardiography Fetal heart disease Maternal–fetal attachment Pregnancy Prenatal attention
1. Introduction Because more than 90% of heart defects occur in fetuses without any known risk factor, fetal echocardiography has become a routine procedure after the twentieth week of pregnancy. In some cases, treatment is performed during pregnancy, and childbirth is assisted by a cardiologist, for immediate neonatal therapy [1]. Visual and audible contact of the parents with the fetus, provided by ultrasound, has the effect of confirming the existence of the child and the ability of the mother to procreate [2,3]. Suspicion of a malformation in the fetus leads to a psychological stress during pregnancy, and anxiety often accompanies the period of diagnosis [4–6]. The information about the abnormality results in anxiety and psychological effects [7,8]. An historical cohort study has demonstrated that fetal echocardiography is a strong predictor for maternal anxiety score [9]. Congenital heart defects constitute a considerable percentage of infant mortality, especially in perinatal and neonatal stages, and are one of the three leading causes of mortality [10]. When a diagnosis of a major congenital cardiac abnormality has been made, important medical and psychological consequences arise [11].
* Corresponding author at: Servic¸o de Psicologia do Instituto de Cardiologia do Rio Grande do Sul/FUC (IC/FUC), Av. Princesa Isabel, 370 Santana, CEP 90.620-000, Porto Alegre, RS, Brazil. Tel.: +55 51 3230 3600. E-mail addresses: [email protected] (P. Ruschel), [email protected] (P. Zielinsky). 0301-2115/$ – see front matter ß 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejogrb.2013.11.029
It has already been shown that levels of anxiety and mood after a diagnosis of fetal malformation could be compared with those of patients with major depressive episodes [12]. When a heart disease was diagnosed in the pre-natal period, mothers reported feeling less responsibility for the defects and tended to improve their marital relationships [13]. Attachment is defined as a persistent desire to search for contact with a significant person, and is fundamental to a healthy development, over the life of the individual. Attachment behaviors, which refer to ways that people use to obtain or maintain proximity between them, are based on this search [14]. Maternal–fetal attachment is defined as the intensity with which women engage in behaviors of care and interaction with their unborn children [15]. There are scarce reports in the literature dealing with instruments to assess maternal–fetal attachment (Maternal Antenatal Attachment Scale [16], and Prenatal Attachment Inventory [17]). The Maternal–Fetal Attachment Scale (MFAS) utilized in this study was constructed based on maternal behavior during pregnancy, familiarity, affection and interaction of the mother with her baby [15]. The MFAS has been validated in Brazil [18] and used to measure maternal attachment during pregnancy. Parental attachment increases in the course of pregnancy. Pregnant women submitted to ultrasound examination show a clearer perception of the fetus, increased maternal–fetal attachment and a more positive health behavior [19]. A Brazilian study assessed women with various fetal malformations, regardless of severity, and compared them to a group
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without this diagnosis. The authors suggested that diagnosis of malformations performed in fetal life decreased maternal–fetal attachment [20]. A phenomenological study with fifteen pregnant women carrying fetuses with non-lethal congenital anomalies pointed in the direction that knowledge of diagnosis did not seem to influence prenatal attachment [21]. Routine psychological interventions with pregnant women whose fetuses were shown by prenatal echocardiography to have a heart defect, over more than 20 years of daily clinical practice in a large tertiary Center of Fetal Cardiology, clearly suggest a different perception, with mothers appearing more attached to their babies. Based on this strong clinical impression and given the important impact of a prenatal cardiac diagnosis upon the mother, the present study was designed to test the hypothesis that the level of maternal–fetal attachment increases after detection of a heart disease in the fetus. 2. Methods This controlled cohort study evaluated women awaiting completion of fetal screening for heart disease. The patients signed an informed consent form, answered a socio-demographic questionnaire and were assessed by the MFAS [15]. The Scale was applied in all pregnant women who underwent screening for fetal heart disease in the Fetal Cardiology Unit of the Institute of Cardiology of Rio Grande do Sul (IC/FUC), during the period between May 2008 and September 2010. After the examination, mothers with a negative diagnosis of fetal heart disease were included in the ‘‘no fetal heart disease’’ (NFHD) group and those with a diagnosis of fetal heart disease (FHD) made up the study group. All pregnant women returned after one month and responded again to the MFAS [15]. The study excluded women with diagnosis of potential improvement of fetal status, diseases incompatible with life and those who did not respond to the second evaluation. The research project was approved by the Research Ethics Committee of IC/FUC. Mothers submitted to the socio-demographic questionnaire provided answers on feelings and perceptions related to pregnancy
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and childbirth. It assessed marital status, education, income, religion, parity, maternal age, planning and issues related to general pregnancy. Feelings and concerns reported by mothers were approached in the questionnaire qualitatively, in a categorical way (yes–no). Good acceptance of pregnancy was considered a positive feeling related to the fact of being pregnant. The MFAS [15], validated for a Brazilian sample, is a Likert scale [22] comprising 24 items, with scores ranging in five levels. The Index scale ranges from 24 to 120 points. In agreement with the cut-off points established by the Brazilian validation, the following levels of maternal–fetal attachment were considered: low (24–47 points), medium (48–97 points) and high (98–120 points). This scale approaches issues related to maternal and fetus interaction, differentiation and attributed characteristics, and evaluates how the mother gives herself to motherhood. The data collected were stored for statistical analysis, which was performed with the PASW 18.0 software. Association between groups and categorical parameters were analyzed by Chi-square test and the comparison of educational level among groups by the non-parametric Mann–Whitney test. For comparison of means among groups Student’s t test was used. The association between initial and final maternal–fetal attachment levels was tested by the McNemar test. The effect size was assessed by the Cohen test for quantitative variables and by odds ratios with 95% confidence intervals for categorical variables. We evaluated 20 mothers who answered the MFAS, with a minimal interval of 24 h and a maximal of 48 h, with two different observers to assess interobserver variability and the same number of mothers answered the questionnaire to the same observer, to assess intraobserver variability. Intraclass coefficients and Bland–Altman plots were then used to analyze reproducibility [23]. 3. Results The scale was applied in 2268 pregnant women prior to fetal echocardiography. A total of 197 pregnant women returned for reassessment after 30 days. They were assigned to two groups
Table 1 Sample characterization – socio-demographic profile of pregnant women.
Marital status (with partner)
NFHD n = 101
FHD n = 96
t(df); x2ðd f Þ ; z
P
80 (79.2)
85 (88.5)
x2ð1Þ ¼ 2:51
0.114
x2ð2Þ ¼ 12:99
0.002
z = 1.15
0.251
x2ð2Þ ¼ 1:83
0.401
x2ð1Þ ¼ 0:00
1.000 0.154 0.911 0.250 0.723 0.936 0.726 0.770 0.247
City Porto Alegre Porto Alegre metropolitan region Other cities in the state
54 (53.5) 31 (30.7) 16 (15.8)
36 (37.5) 23 (24.0) 37 (38.5)
Education Illiterate Incomplete primary Complete primary Incomplete high school High school Superior
2 17 11 25 31 15
0 24 17 14 30 11
Income (minimum wages) 6
72 (71.3) 20 (19.8) 9 (8.9)
71 (74) 21 (21.9) 4 (4.2)
Religious Age of mother (years) Gestational age (weeks) Primiparous Loss of child Planning Good acceptance Name chosen Concerns with the baby
83 (82.2) 27.61 6.40 26.67 (4.17) 46 (45.5) 18 (17.8) 50 (49.5) 78 (77.2) 87 (86.1) 99 (98.0)
78 (81.3) 28.97 6.89 26.74 (4.19) 35 (36.5) 20 (20.8) 46 (47.9) 72 (75.0) 85 (88.5) 90 (93.8)
(2.0) (18.2) (10.9) (24.8) (30.7) (14.8)
(0.0) (25.0) (17.7) (14.6) (31.3) (11.5)
t(195) = 1.43 t(195) = 0.11 x2ð1Þ ¼ 0:11 x2ð1Þ ¼ 0:13 x2ð1Þ ¼ 0:01 x2ð1Þ ¼ 0:04 x2ð1Þ ¼ 0:09 x2ð1Þ ¼ 1:34
NFHD: none fetal heart disease; FHD: fetal heart disease; n (%); mean SD; t(dg): t test (degrees of freedom); x2ðd f Þ : Chi-square; z: Mann–Whitney.
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Fig. 1. Number of cases of different fetal heart defects. AoA: aortic atresia; PA: pulmonary atresia; AVB: atrioventricular block; VSD: ventricular septal defect; AoCo: aortic coarctation; DlMi: double mitral lesion; DORV: double outlet right ventricle; AVSD: atrioventricular septal defect; AoS: aortic stenosis; PS: pulmonary stenosis; RVH, right ventricular hypoplasia; LVH, left ventricular hypoplasia; IAA: interrupted aortic arch; Shone S: Shone syndrome; T. Fallot: Tetralogy of Fallot; TGV: transposition of great vessels.
according to the presence (FHD group, n = 96) or absence (NFHD group, n = 101) of fetal cardiac abnormalities. The characterization of groups according to variables showed that the groups differ only by city of origin (Table 1). The effect size for gestational and maternal ages differences was low (Cohen’s d = 0.205 and 0.017 respectively). Fig. 1 shows the distribution of cardiac abnormalities diagnosed in the FHD group. The results show a significant increase in the level of maternal–fetal attachment after the diagnosis of fetal heart disease, as assessed 30 days after screening. The mean attachment level of the 2268 pregnant women was 85.2 9.1. Before the screening, the MFAS [15] results showed a mean maternal–fetal attachment level of 94.7 9.7, with no significant
difference between the groups. After thirty days, a significant difference (p = 0.003, Chi-square test) was observed between the two groups. The mean level of attachment was 95.5 10 in the NFHD group and 99.51 8.91 in the FHD group. As shown in Fig. 2, the analysis of attachment among groups, classified by levels, and performed in the initial (before screening for fetal heart disease) and late (30 days after the examination) periods, showed no significant difference between the groups in the distribution of baseline attachment levels in pregnant women (p = 0.081, Chi-square test, odds ratio = 1.74 (95% CI = 0.98–3.09). On the other hand, in the final period the difference between the migration from medium to high level was significantly higher in the FHD group (p = 0.017, Chi-square test, odds ratio = 2.08 (95% CI = 1.18–3.69).
Fig. 2. Comparison of initial and final levels of maternal–fetal attachment. NFHD: non-fetal heart disease; FHD: fetal heart disease. *Chi-square test.
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Fig. 3. Comparison of the level of maternal–fetal attachment in case and control mothers. NFHD: non-fetal heart disease, FHD: fetal heart disease. *McNemar test.
Table 2 Feelings that pregnant women think they will have during childbirth. Feelings
NFHD
FHD
x2ð1Þ
P
Insecurity Fear Doubt Tranquility Pain Nervousness Happiness
34 39 25 46 48 60 66
49 48 37 44 53 61 54
4.15 2.15 3.72 0.00 0.88 0.20 1.35
0.042 0.143 0.054 1.000 0.349 0.653 0.245
(33.7) (38.6) (24.8) (45.5) (47.5) (59.4) (65.3)
(51.0) (50.0) (38.5) (45.8) (55.2) (63.5) (56.3)
NFHD: none fetal heart disease; FHD: fetal heart disease; n (%); x2 : Chi-square.
Table 3 Logistic regressive multivariate analysis of predictive variables of high-fetal attachment. Variables
Odds ratio
95% Confidence interval
P
Fetal heart defect Feeling pain in childbirth Hypertension Planning for child
2.19 1.94 4.70 1.85
1.21–3.98 1.07–3.51 1.23–17.96 1.02–3.37
0.010 0.028 0.024 0.044
The intra-group evaluation (Fig. 3) showed that the transition from medium to high level of attachment, analyzed in the initial and final periods, was more striking in the FHD group (p = 0.009, McNemar test) than in the NFHD group (p = 0.050, McNemar test). The socio-demographic questionnaire, which evaluated the characteristics of pregnancy, provided data on the anticipated feelings the mothers expressed in relation to the upcoming labor. Women in the FHD group showed higher levels of insecurity and doubts than NFHD women (p = 0.042 and p = 0.054, respectively, Student t test) (Table 2). Table 3 presents the result of multivariate analysis, which showed a higher rate of attachment in the FHD group. The variables imagining a sensation of pain during childbirth, high blood pressure and having planned the child were also predictive of a high level of attachment. The reproducibility of the MFAS used in the study was determined. High intra-class correlation coefficients for interobserver and intra-observer agreement were observed (0.98 [CI:
Fig. 4. Interobserver concordance.
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P. Ruschel et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 174 (2014) 70–75
Fig. 5. Intraobserver concordance.
0.95–0.99] and 0.97 [CI: 0.93–0.99] respectively), as expressed by the Bland–Altman plots in Figs. 4 and 5. 4. Comments The results of this study show that the diagnosis of heart disease in fetal life increases maternal–fetal attachment. The variation of the level of attachment in the groups with and without fetal diagnosis of heart disease was evaluated before fetal echocardiography and 30 days later. This time interval was considered appropriate for the mother to establish a pattern of relationship with the fetus after diagnosis of congenital heart disease. Our study confirms previous data that maternal–fetal attachment increases over pregnancy [19], although we have found an important and significant increase of attachment in the group with a fetal cardiac diagnosis. In this study, diagnosis of fetal heart disease had the effect of warning the mother about the fetal health compromise. In the total sample, no score was classified as low level of attachment, showing that all pregnant women who presented to routine fetal heart screening showed at least a medium level of attachment. Migration from the initial medium level of attachment to a high level was observed in 21.8% of mothers the NFHD group, and in 26.9% of the FHD group, indicating that a diagnosis of heart disease during fetal life results in an increase of maternal–fetal attachment. The results of the present study differ from a previous report [20], performed with the same scale of attachment, which suggested that the diagnosis of fetal malformations in life resulted in a reduction of maternal–fetal attachment. That report included a number of different fetal malformations, unlike the present study, in which heart diseases incompatible with life as well as noncardiac malformations were excluded. The presence of heart defects not compatible with life could explain the decrease in maternal–fetal attachment observed in that study. These considerations strongly support the idea that the mother is motivated to protect the baby with malformations compatible with life, thus increasing her attachment to it. In another study, the investigation of the levels of attachment of pregnant women to fetuses diagnosed with malformations showed that high levels of maternal–fetal attachment were not reached in the presence of lethal fetal malformation. These results support the perception that diagnosis of a lethal defect has a different effect than when there are chances of survival for the baby [24], as in the present study.
The analysis of socio-demographic characteristics of the sample showed that the group with fetal cardiac diagnosis was made up of a higher number of women who came from smaller cities to have fetal echocardiography performed. This group showed higher levels of maternal–fetal attachment in the initial assessment, not significant when compared to the control group. These findings raise the hypothesis that a previously suspected diagnosis of possible fetal heart disease has already induced greater attachment in women of this group, who were then referred to a tertiary center for confirmation of the diagnosis. The results also showed a significant difference in the feelings expected for childbirth when the two groups were compared, with the mothers of the FHD group characterized by expecting feelings of doubts and insecurity. Since this issue was sought in both groups at first assessment, before the screening for fetal heart disease, it is possible that these mothers were more sensitive than those of the NFHD group, possibly due to a higher prevalence of already suspected fetal heart disease, as mentioned before. Multivariate analysis was used to identify variables that could predict a high level of maternal–fetal attachment. The following variables were shown to be predictive: diagnosis of fetal heart disease, fear of feeling pain in childbirth, arterial hypertension and previous planning of pregnancy. For the mother, from a psychoanalytic point of view, a child is destined to fulfill a task of filling a gap in the deep feeling of subjective identity. When a different baby is generated, parents will be faced with the lack of ‘‘something’’ [25]. Illness or imperfection of a child may represent a threat to the psychic integrity of the couple [26], confronting their own narcissism and sexual maturation [27]. The diagnosis of fetal abnormality frequently results in a decrease in maternal self-esteem, in feelings of helplessness, and in the search for the cause of the disease [28], implying the need for parents to mourn the loss of the ideal son [29–31]. The literature also describes this grief as a feeling directed to the newborn, who is at risk of life [32]. According to the literature, the fear of pain in childbirth, which was confirmed as a predictor of increase in maternal–fetal attachment, may be seen as the first milestone of maternity. It is also referred to as a price to be paid for receiving the award, which is the child. Another point of view states that in the minds of some women, the good mother must feel pain while she gives birth in order to fulfill her role. For some pregnant women, pain is seen as suffering, and analgesia as salvation. For others, however, the pain of labor is seen as the true maternity [33]. The third variable that was found as a predictor of increased level of maternal–fetal attachment is high blood pressure. Previous studies have shown that the psychological aspects most commonly found in the binomial heart disease and pregnancy are fear of complications such as not enduring pregnancy, failure of the heart during labor and death [34]. The risk factor in pregnancy may induce in the mother a new type of fear, for herself and her son, for what is happening in her body, or for the child’ abnormalities, beyond the fear of loss of control in relation to pregnancy and herself [35]. Planning of pregnancy was also a predictor of increased maternal–fetal attachment. Pregnancy results in several changes in the life of the woman: inevitable physical changes, need to organize the home to receive the new baby, and the inclusion of a third person in the relationship of the couple. Our results show that planning of pregnancy, i.e., being in a period of life which is adequate for pregnancy, provides greater maternal–fetal attachment, as already suggested in a previous study [36]. A potential selection bias in our study could be represented by the inclusion of pregnant women referred with a suspicion of fetal heart abnormality. The results show, however, that even if the initial attachment was already increased due to suspicion of heart
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disease, a significant increase in maternal–fetal attachment occurred after confirmation of diagnosis. The reproducibility of the scale used was excellent, thus controlling potential measurement biases. Multivariate analysis considered the possible confounding factors affecting the levels of maternal–fetal attachment, represented, as mentioned above, by maternal hypertension, fear of pain in childbirth and pregnancy planning. In conclusion, the level of maternal–fetal attachment is more evident in mothers after knowing that her fetus is affected by a cardiac abnormality than in the absence of this condition. Conflict of interest None of the authors has a conflict of interest. References [1] Zielinsky P. Cardiologia Fetal cieˆncia e pra´tica. Rio de Janeiro: Revinter; 2006. [2] Grigoletti L. A influeˆncia da ultrassonografia na representac¸a˜o do filho imagina´rio-filho real. Psico 2005;36:149–57. [3] Gomes AG. A ultra-sonografia obste´trica e suas Implicac¸o˜es na relac¸a˜o ma˜efeto: Impresso˜es e sentimentos de gestantes com e sem diagno´stico de anormalidade fetal.[dissertac¸a˜o] Porto Alegre: Universidade Federal do Rio Grande do Sul; 2003. [4] Kowalcek I. Stress and anxiety associated with prenatal diagnosis. Best Pract Res Clin Obstet Gynaecol 2007;21:221–8. [5] Kowalcek I, Lammers C, Brunk J, Bieniakiewicz I, Gembruch U. Fears of pregnant women if prenatal examination yields or does not yield any findings. Zbl Gynakol 2002;124:170–5. [6] Kleinveld JH, Timmermans DR, de Smit DJ, Ade´r HJ, van der Wal G, ten Kate LP. Does prenatal screening influence anxiety levels of pregnant women? A longitudinal randomised controlled trial. Prenat Diagn 2006;26:354–61. [7] Larsson AK, Svalenius EC, Lundqvist A, Dykes AK. Parents´ experiences of abnormal ultrasound examination – vacillating between emotional confusion and sense of reality. Reprod Health 2010;7:10. [8] Brosig C, Whitstone B, Frommelt M, Frisbee S, Leuthner S. Psychological distress in parents of children with severe congenital heart disease: the impact of prenatal versus postnatal diagnosis. J Perinatol 2007;27:687–92. [9] Rosenberg KB, Monk C, Kleinman CS, et al. Referral for fetal echocardiography is associated with increased maternal anxiety. J Psychosom Obstet Gynaecol 2010;31:60–9. [10] Guerchicoff M, Marantz P, Infante J. Evaluacio´n del impacto del diagno´stico precoz de las cardiopatı´as conge´nitas. Arch Argent Pediatr 2004;102:445–50. [11] Sholler GF, Kasparian NA, Pye VE, Cole AD, Winlaw DS. Fetal and post-natal diagnosis of major congenital heart disease: implications for medical and psychological care in the current era. J Paediatr Child Health 2011;47:717–22. [12] Leithner K, Maar A, Fischer-Kern M, Hilger E, Lo¨ffler-Stastka H, Ponocny-Seliger E. Affective state of women following a prenatal diagnosis: predictors of a negative psychological outcome. Ultrasound Obstet Gynecol 2004;23:240–6. [13] Sklansky M, Tang A, Levy D, et al. Maternal psychological impact of fetal echocardiography. J Am Soc Echocardiogr 2002;15:159–66.
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Contents lists available at ScienceDirect
European Journal of Obstetrics & Gynecology and Reproductive Biology journal homepage: www.elsevier.com/locate/ejogrb
Maternal–fetal attachment and prenatal diagnosis of heart disease Patricia Ruschel *, Paulo Zielinsky, Cristiane Grings, Julia Pimentel, Liege Azevedo, Rafaele Paniagua, Luiz H. Nicoloso Fetal Cardiology Unit, Instituto de Cardiologia do Rio Grande do Sul/Fundac¸a˜o Universita´ria de Cardiologia, Porto Alegre, Brazil
A R T I C L E I N F O
A B S T R A C T
Article history: Received 13 May 2013 Received in revised form 9 November 2013 Accepted 25 November 2013
Objective: To test the hypothesis that there are differences in the level of maternal–fetal attachment before and after fetal echocardiography in the presence or absence of cardiac abnormalities. Study design: Cohort study in which the mothers responded to a validated Maternal–Fetal Attachment Scale. The study compared a group of pregnant women with diagnosis of fetal heart disease (FHD) with a group without this diagnosis (‘‘no fetal heart disease’’ – NFHD). Results: 197 pregnant women were included, 96 FHD and 101 NFHD. Maternal–fetal attachment at the initial and final periods showed no significant baseline differences between groups (p = 0.081). At the final period, migration from medium to high level of attachment was significantly higher in FHD (p = 0.017). Transition from medium to high levels comparing the initial and final periods was more pronounced in FHD (p = 0.009). Conclusion: Diagnosis of fetal heart disease increases the level of maternal–fetal attachment. ß 2013 Elsevier Ireland Ltd. All rights reserved.
Keywords: Fetal echocardiography Fetal heart disease Maternal–fetal attachment Pregnancy Prenatal attention
1. Introduction Because more than 90% of heart defects occur in fetuses without any known risk factor, fetal echocardiography has become a routine procedure after the twentieth week of pregnancy. In some cases, treatment is performed during pregnancy, and childbirth is assisted by a cardiologist, for immediate neonatal therapy [1]. Visual and audible contact of the parents with the fetus, provided by ultrasound, has the effect of confirming the existence of the child and the ability of the mother to procreate [2,3]. Suspicion of a malformation in the fetus leads to a psychological stress during pregnancy, and anxiety often accompanies the period of diagnosis [4–6]. The information about the abnormality results in anxiety and psychological effects [7,8]. An historical cohort study has demonstrated that fetal echocardiography is a strong predictor for maternal anxiety score [9]. Congenital heart defects constitute a considerable percentage of infant mortality, especially in perinatal and neonatal stages, and are one of the three leading causes of mortality [10]. When a diagnosis of a major congenital cardiac abnormality has been made, important medical and psychological consequences arise [11].
* Corresponding author at: Servic¸o de Psicologia do Instituto de Cardiologia do Rio Grande do Sul/FUC (IC/FUC), Av. Princesa Isabel, 370 Santana, CEP 90.620-000, Porto Alegre, RS, Brazil. Tel.: +55 51 3230 3600. E-mail addresses: [email protected] (P. Ruschel), [email protected] (P. Zielinsky). 0301-2115/$ – see front matter ß 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejogrb.2013.11.029
It has already been shown that levels of anxiety and mood after a diagnosis of fetal malformation could be compared with those of patients with major depressive episodes [12]. When a heart disease was diagnosed in the pre-natal period, mothers reported feeling less responsibility for the defects and tended to improve their marital relationships [13]. Attachment is defined as a persistent desire to search for contact with a significant person, and is fundamental to a healthy development, over the life of the individual. Attachment behaviors, which refer to ways that people use to obtain or maintain proximity between them, are based on this search [14]. Maternal–fetal attachment is defined as the intensity with which women engage in behaviors of care and interaction with their unborn children [15]. There are scarce reports in the literature dealing with instruments to assess maternal–fetal attachment (Maternal Antenatal Attachment Scale [16], and Prenatal Attachment Inventory [17]). The Maternal–Fetal Attachment Scale (MFAS) utilized in this study was constructed based on maternal behavior during pregnancy, familiarity, affection and interaction of the mother with her baby [15]. The MFAS has been validated in Brazil [18] and used to measure maternal attachment during pregnancy. Parental attachment increases in the course of pregnancy. Pregnant women submitted to ultrasound examination show a clearer perception of the fetus, increased maternal–fetal attachment and a more positive health behavior [19]. A Brazilian study assessed women with various fetal malformations, regardless of severity, and compared them to a group
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without this diagnosis. The authors suggested that diagnosis of malformations performed in fetal life decreased maternal–fetal attachment [20]. A phenomenological study with fifteen pregnant women carrying fetuses with non-lethal congenital anomalies pointed in the direction that knowledge of diagnosis did not seem to influence prenatal attachment [21]. Routine psychological interventions with pregnant women whose fetuses were shown by prenatal echocardiography to have a heart defect, over more than 20 years of daily clinical practice in a large tertiary Center of Fetal Cardiology, clearly suggest a different perception, with mothers appearing more attached to their babies. Based on this strong clinical impression and given the important impact of a prenatal cardiac diagnosis upon the mother, the present study was designed to test the hypothesis that the level of maternal–fetal attachment increases after detection of a heart disease in the fetus. 2. Methods This controlled cohort study evaluated women awaiting completion of fetal screening for heart disease. The patients signed an informed consent form, answered a socio-demographic questionnaire and were assessed by the MFAS [15]. The Scale was applied in all pregnant women who underwent screening for fetal heart disease in the Fetal Cardiology Unit of the Institute of Cardiology of Rio Grande do Sul (IC/FUC), during the period between May 2008 and September 2010. After the examination, mothers with a negative diagnosis of fetal heart disease were included in the ‘‘no fetal heart disease’’ (NFHD) group and those with a diagnosis of fetal heart disease (FHD) made up the study group. All pregnant women returned after one month and responded again to the MFAS [15]. The study excluded women with diagnosis of potential improvement of fetal status, diseases incompatible with life and those who did not respond to the second evaluation. The research project was approved by the Research Ethics Committee of IC/FUC. Mothers submitted to the socio-demographic questionnaire provided answers on feelings and perceptions related to pregnancy
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and childbirth. It assessed marital status, education, income, religion, parity, maternal age, planning and issues related to general pregnancy. Feelings and concerns reported by mothers were approached in the questionnaire qualitatively, in a categorical way (yes–no). Good acceptance of pregnancy was considered a positive feeling related to the fact of being pregnant. The MFAS [15], validated for a Brazilian sample, is a Likert scale [22] comprising 24 items, with scores ranging in five levels. The Index scale ranges from 24 to 120 points. In agreement with the cut-off points established by the Brazilian validation, the following levels of maternal–fetal attachment were considered: low (24–47 points), medium (48–97 points) and high (98–120 points). This scale approaches issues related to maternal and fetus interaction, differentiation and attributed characteristics, and evaluates how the mother gives herself to motherhood. The data collected were stored for statistical analysis, which was performed with the PASW 18.0 software. Association between groups and categorical parameters were analyzed by Chi-square test and the comparison of educational level among groups by the non-parametric Mann–Whitney test. For comparison of means among groups Student’s t test was used. The association between initial and final maternal–fetal attachment levels was tested by the McNemar test. The effect size was assessed by the Cohen test for quantitative variables and by odds ratios with 95% confidence intervals for categorical variables. We evaluated 20 mothers who answered the MFAS, with a minimal interval of 24 h and a maximal of 48 h, with two different observers to assess interobserver variability and the same number of mothers answered the questionnaire to the same observer, to assess intraobserver variability. Intraclass coefficients and Bland–Altman plots were then used to analyze reproducibility [23]. 3. Results The scale was applied in 2268 pregnant women prior to fetal echocardiography. A total of 197 pregnant women returned for reassessment after 30 days. They were assigned to two groups
Table 1 Sample characterization – socio-demographic profile of pregnant women.
Marital status (with partner)
NFHD n = 101
FHD n = 96
t(df); x2ðd f Þ ; z
P
80 (79.2)
85 (88.5)
x2ð1Þ ¼ 2:51
0.114
x2ð2Þ ¼ 12:99
0.002
z = 1.15
0.251
x2ð2Þ ¼ 1:83
0.401
x2ð1Þ ¼ 0:00
1.000 0.154 0.911 0.250 0.723 0.936 0.726 0.770 0.247
City Porto Alegre Porto Alegre metropolitan region Other cities in the state
54 (53.5) 31 (30.7) 16 (15.8)
36 (37.5) 23 (24.0) 37 (38.5)
Education Illiterate Incomplete primary Complete primary Incomplete high school High school Superior
2 17 11 25 31 15
0 24 17 14 30 11
Income (minimum wages) 6
72 (71.3) 20 (19.8) 9 (8.9)
71 (74) 21 (21.9) 4 (4.2)
Religious Age of mother (years) Gestational age (weeks) Primiparous Loss of child Planning Good acceptance Name chosen Concerns with the baby
83 (82.2) 27.61 6.40 26.67 (4.17) 46 (45.5) 18 (17.8) 50 (49.5) 78 (77.2) 87 (86.1) 99 (98.0)
78 (81.3) 28.97 6.89 26.74 (4.19) 35 (36.5) 20 (20.8) 46 (47.9) 72 (75.0) 85 (88.5) 90 (93.8)
(2.0) (18.2) (10.9) (24.8) (30.7) (14.8)
(0.0) (25.0) (17.7) (14.6) (31.3) (11.5)
t(195) = 1.43 t(195) = 0.11 x2ð1Þ ¼ 0:11 x2ð1Þ ¼ 0:13 x2ð1Þ ¼ 0:01 x2ð1Þ ¼ 0:04 x2ð1Þ ¼ 0:09 x2ð1Þ ¼ 1:34
NFHD: none fetal heart disease; FHD: fetal heart disease; n (%); mean SD; t(dg): t test (degrees of freedom); x2ðd f Þ : Chi-square; z: Mann–Whitney.
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Fig. 1. Number of cases of different fetal heart defects. AoA: aortic atresia; PA: pulmonary atresia; AVB: atrioventricular block; VSD: ventricular septal defect; AoCo: aortic coarctation; DlMi: double mitral lesion; DORV: double outlet right ventricle; AVSD: atrioventricular septal defect; AoS: aortic stenosis; PS: pulmonary stenosis; RVH, right ventricular hypoplasia; LVH, left ventricular hypoplasia; IAA: interrupted aortic arch; Shone S: Shone syndrome; T. Fallot: Tetralogy of Fallot; TGV: transposition of great vessels.
according to the presence (FHD group, n = 96) or absence (NFHD group, n = 101) of fetal cardiac abnormalities. The characterization of groups according to variables showed that the groups differ only by city of origin (Table 1). The effect size for gestational and maternal ages differences was low (Cohen’s d = 0.205 and 0.017 respectively). Fig. 1 shows the distribution of cardiac abnormalities diagnosed in the FHD group. The results show a significant increase in the level of maternal–fetal attachment after the diagnosis of fetal heart disease, as assessed 30 days after screening. The mean attachment level of the 2268 pregnant women was 85.2 9.1. Before the screening, the MFAS [15] results showed a mean maternal–fetal attachment level of 94.7 9.7, with no significant
difference between the groups. After thirty days, a significant difference (p = 0.003, Chi-square test) was observed between the two groups. The mean level of attachment was 95.5 10 in the NFHD group and 99.51 8.91 in the FHD group. As shown in Fig. 2, the analysis of attachment among groups, classified by levels, and performed in the initial (before screening for fetal heart disease) and late (30 days after the examination) periods, showed no significant difference between the groups in the distribution of baseline attachment levels in pregnant women (p = 0.081, Chi-square test, odds ratio = 1.74 (95% CI = 0.98–3.09). On the other hand, in the final period the difference between the migration from medium to high level was significantly higher in the FHD group (p = 0.017, Chi-square test, odds ratio = 2.08 (95% CI = 1.18–3.69).
Fig. 2. Comparison of initial and final levels of maternal–fetal attachment. NFHD: non-fetal heart disease; FHD: fetal heart disease. *Chi-square test.
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Fig. 3. Comparison of the level of maternal–fetal attachment in case and control mothers. NFHD: non-fetal heart disease, FHD: fetal heart disease. *McNemar test.
Table 2 Feelings that pregnant women think they will have during childbirth. Feelings
NFHD
FHD
x2ð1Þ
P
Insecurity Fear Doubt Tranquility Pain Nervousness Happiness
34 39 25 46 48 60 66
49 48 37 44 53 61 54
4.15 2.15 3.72 0.00 0.88 0.20 1.35
0.042 0.143 0.054 1.000 0.349 0.653 0.245
(33.7) (38.6) (24.8) (45.5) (47.5) (59.4) (65.3)
(51.0) (50.0) (38.5) (45.8) (55.2) (63.5) (56.3)
NFHD: none fetal heart disease; FHD: fetal heart disease; n (%); x2 : Chi-square.
Table 3 Logistic regressive multivariate analysis of predictive variables of high-fetal attachment. Variables
Odds ratio
95% Confidence interval
P
Fetal heart defect Feeling pain in childbirth Hypertension Planning for child
2.19 1.94 4.70 1.85
1.21–3.98 1.07–3.51 1.23–17.96 1.02–3.37
0.010 0.028 0.024 0.044
The intra-group evaluation (Fig. 3) showed that the transition from medium to high level of attachment, analyzed in the initial and final periods, was more striking in the FHD group (p = 0.009, McNemar test) than in the NFHD group (p = 0.050, McNemar test). The socio-demographic questionnaire, which evaluated the characteristics of pregnancy, provided data on the anticipated feelings the mothers expressed in relation to the upcoming labor. Women in the FHD group showed higher levels of insecurity and doubts than NFHD women (p = 0.042 and p = 0.054, respectively, Student t test) (Table 2). Table 3 presents the result of multivariate analysis, which showed a higher rate of attachment in the FHD group. The variables imagining a sensation of pain during childbirth, high blood pressure and having planned the child were also predictive of a high level of attachment. The reproducibility of the MFAS used in the study was determined. High intra-class correlation coefficients for interobserver and intra-observer agreement were observed (0.98 [CI:
Fig. 4. Interobserver concordance.
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Fig. 5. Intraobserver concordance.
0.95–0.99] and 0.97 [CI: 0.93–0.99] respectively), as expressed by the Bland–Altman plots in Figs. 4 and 5. 4. Comments The results of this study show that the diagnosis of heart disease in fetal life increases maternal–fetal attachment. The variation of the level of attachment in the groups with and without fetal diagnosis of heart disease was evaluated before fetal echocardiography and 30 days later. This time interval was considered appropriate for the mother to establish a pattern of relationship with the fetus after diagnosis of congenital heart disease. Our study confirms previous data that maternal–fetal attachment increases over pregnancy [19], although we have found an important and significant increase of attachment in the group with a fetal cardiac diagnosis. In this study, diagnosis of fetal heart disease had the effect of warning the mother about the fetal health compromise. In the total sample, no score was classified as low level of attachment, showing that all pregnant women who presented to routine fetal heart screening showed at least a medium level of attachment. Migration from the initial medium level of attachment to a high level was observed in 21.8% of mothers the NFHD group, and in 26.9% of the FHD group, indicating that a diagnosis of heart disease during fetal life results in an increase of maternal–fetal attachment. The results of the present study differ from a previous report [20], performed with the same scale of attachment, which suggested that the diagnosis of fetal malformations in life resulted in a reduction of maternal–fetal attachment. That report included a number of different fetal malformations, unlike the present study, in which heart diseases incompatible with life as well as noncardiac malformations were excluded. The presence of heart defects not compatible with life could explain the decrease in maternal–fetal attachment observed in that study. These considerations strongly support the idea that the mother is motivated to protect the baby with malformations compatible with life, thus increasing her attachment to it. In another study, the investigation of the levels of attachment of pregnant women to fetuses diagnosed with malformations showed that high levels of maternal–fetal attachment were not reached in the presence of lethal fetal malformation. These results support the perception that diagnosis of a lethal defect has a different effect than when there are chances of survival for the baby [24], as in the present study.
The analysis of socio-demographic characteristics of the sample showed that the group with fetal cardiac diagnosis was made up of a higher number of women who came from smaller cities to have fetal echocardiography performed. This group showed higher levels of maternal–fetal attachment in the initial assessment, not significant when compared to the control group. These findings raise the hypothesis that a previously suspected diagnosis of possible fetal heart disease has already induced greater attachment in women of this group, who were then referred to a tertiary center for confirmation of the diagnosis. The results also showed a significant difference in the feelings expected for childbirth when the two groups were compared, with the mothers of the FHD group characterized by expecting feelings of doubts and insecurity. Since this issue was sought in both groups at first assessment, before the screening for fetal heart disease, it is possible that these mothers were more sensitive than those of the NFHD group, possibly due to a higher prevalence of already suspected fetal heart disease, as mentioned before. Multivariate analysis was used to identify variables that could predict a high level of maternal–fetal attachment. The following variables were shown to be predictive: diagnosis of fetal heart disease, fear of feeling pain in childbirth, arterial hypertension and previous planning of pregnancy. For the mother, from a psychoanalytic point of view, a child is destined to fulfill a task of filling a gap in the deep feeling of subjective identity. When a different baby is generated, parents will be faced with the lack of ‘‘something’’ [25]. Illness or imperfection of a child may represent a threat to the psychic integrity of the couple [26], confronting their own narcissism and sexual maturation [27]. The diagnosis of fetal abnormality frequently results in a decrease in maternal self-esteem, in feelings of helplessness, and in the search for the cause of the disease [28], implying the need for parents to mourn the loss of the ideal son [29–31]. The literature also describes this grief as a feeling directed to the newborn, who is at risk of life [32]. According to the literature, the fear of pain in childbirth, which was confirmed as a predictor of increase in maternal–fetal attachment, may be seen as the first milestone of maternity. It is also referred to as a price to be paid for receiving the award, which is the child. Another point of view states that in the minds of some women, the good mother must feel pain while she gives birth in order to fulfill her role. For some pregnant women, pain is seen as suffering, and analgesia as salvation. For others, however, the pain of labor is seen as the true maternity [33]. The third variable that was found as a predictor of increased level of maternal–fetal attachment is high blood pressure. Previous studies have shown that the psychological aspects most commonly found in the binomial heart disease and pregnancy are fear of complications such as not enduring pregnancy, failure of the heart during labor and death [34]. The risk factor in pregnancy may induce in the mother a new type of fear, for herself and her son, for what is happening in her body, or for the child’ abnormalities, beyond the fear of loss of control in relation to pregnancy and herself [35]. Planning of pregnancy was also a predictor of increased maternal–fetal attachment. Pregnancy results in several changes in the life of the woman: inevitable physical changes, need to organize the home to receive the new baby, and the inclusion of a third person in the relationship of the couple. Our results show that planning of pregnancy, i.e., being in a period of life which is adequate for pregnancy, provides greater maternal–fetal attachment, as already suggested in a previous study [36]. A potential selection bias in our study could be represented by the inclusion of pregnant women referred with a suspicion of fetal heart abnormality. The results show, however, that even if the initial attachment was already increased due to suspicion of heart
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disease, a significant increase in maternal–fetal attachment occurred after confirmation of diagnosis. The reproducibility of the scale used was excellent, thus controlling potential measurement biases. Multivariate analysis considered the possible confounding factors affecting the levels of maternal–fetal attachment, represented, as mentioned above, by maternal hypertension, fear of pain in childbirth and pregnancy planning. In conclusion, the level of maternal–fetal attachment is more evident in mothers after knowing that her fetus is affected by a cardiac abnormality than in the absence of this condition. Conflict of interest None of the authors has a conflict of interest. References [1] Zielinsky P. Cardiologia Fetal cieˆncia e pra´tica. Rio de Janeiro: Revinter; 2006. [2] Grigoletti L. A influeˆncia da ultrassonografia na representac¸a˜o do filho imagina´rio-filho real. Psico 2005;36:149–57. [3] Gomes AG. A ultra-sonografia obste´trica e suas Implicac¸o˜es na relac¸a˜o ma˜efeto: Impresso˜es e sentimentos de gestantes com e sem diagno´stico de anormalidade fetal.[dissertac¸a˜o] Porto Alegre: Universidade Federal do Rio Grande do Sul; 2003. [4] Kowalcek I. Stress and anxiety associated with prenatal diagnosis. Best Pract Res Clin Obstet Gynaecol 2007;21:221–8. [5] Kowalcek I, Lammers C, Brunk J, Bieniakiewicz I, Gembruch U. Fears of pregnant women if prenatal examination yields or does not yield any findings. Zbl Gynakol 2002;124:170–5. [6] Kleinveld JH, Timmermans DR, de Smit DJ, Ade´r HJ, van der Wal G, ten Kate LP. Does prenatal screening influence anxiety levels of pregnant women? A longitudinal randomised controlled trial. Prenat Diagn 2006;26:354–61. [7] Larsson AK, Svalenius EC, Lundqvist A, Dykes AK. Parents´ experiences of abnormal ultrasound examination – vacillating between emotional confusion and sense of reality. Reprod Health 2010;7:10. [8] Brosig C, Whitstone B, Frommelt M, Frisbee S, Leuthner S. Psychological distress in parents of children with severe congenital heart disease: the impact of prenatal versus postnatal diagnosis. J Perinatol 2007;27:687–92. [9] Rosenberg KB, Monk C, Kleinman CS, et al. Referral for fetal echocardiography is associated with increased maternal anxiety. J Psychosom Obstet Gynaecol 2010;31:60–9. [10] Guerchicoff M, Marantz P, Infante J. Evaluacio´n del impacto del diagno´stico precoz de las cardiopatı´as conge´nitas. Arch Argent Pediatr 2004;102:445–50. [11] Sholler GF, Kasparian NA, Pye VE, Cole AD, Winlaw DS. Fetal and post-natal diagnosis of major congenital heart disease: implications for medical and psychological care in the current era. J Paediatr Child Health 2011;47:717–22. [12] Leithner K, Maar A, Fischer-Kern M, Hilger E, Lo¨ffler-Stastka H, Ponocny-Seliger E. Affective state of women following a prenatal diagnosis: predictors of a negative psychological outcome. Ultrasound Obstet Gynecol 2004;23:240–6. [13] Sklansky M, Tang A, Levy D, et al. Maternal psychological impact of fetal echocardiography. J Am Soc Echocardiogr 2002;15:159–66.
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