Post-breastfeeding stress response and breastfeeding selfe � cacy as modi � able predictors of exclusive breastfeeding at 3 months postpartum : a longitudinal study


 Background: The prevalence of exclusive breastfeeding of infants at 3 months postpartum is only 50% in Japan. In order to increase this rate, we aimed to examine modifiable factors related to exclusive breastfeeding at 3 months postpartum by focusing on breastfeeding-related and psychosocial variables at 1 month postpartum. Methods: This prospective cohort study was conducted in a secondary medical care center in Osaka, Japan from February 2017 to October 2018. Demographic variables, infant feeding modality, breastfeeding-related variables, and psychosocial variables were obtained using questionnaires at 1 month postpartum. Daytime salivary cortisol levels before and after breastfeeding at 1 month postpartum were measured as a biological marker for stress responses associated with breastfeeding. Each infant’s feeding modality was re-assessed at 3 months postpartum. Multiple logistic regression analyses were performed to examine the factors affecting exclusive breastfeeding at 3 months postpartum. Results: Of the 104 participants, 61 reported exclusive breastfeeding at 3 months postpartum. The following factors were significantly associated with exclusive breastfeeding at 3 months postpartum: multiparity (adjusted odds ratio, 95% confidence interval: 11.13, 2.08–59.59), having a university degree (5.25, 1.04–26.53), no plan to return to work by 6 months postpartum (0.02, 0.00–0.46), exclusive breastfeeding at 1 month postpartum (42.84, 6.05–303.52), lower cortisol level after breastfeeding at 1 month postpartum (0.00, 0.00–0.02), and higher breastfeeding self-efficacy scale score at 1 month postpartum (1.07, 1.00–1.14). In parity-specific analyses, exclusive breastfeeding (25.33, 4.75–134.98) and lower cortisol level after breastfeeding (0.00, 0.00–0.21) at 1 month postpartum in primiparous women, and lower cortisol level after breastfeeding (0.00, 0.00–0.94), higher breastfeeding self-efficacy score (1.18, 1.05–1.32), and absence of breast complications (0.09, 0.01-0.82) at 1 month postpartum in multiparous women were associated with exclusive breastfeeding at 3 months postpartum. Conclusions: Stress levels after breastfeeding, breastfeeding self-efficacy, and presence of breast complications could be modifiable factors related to subsequent exclusive breastfeeding. Further research is needed to examine whether approaches to reducing breastfeeding-related stress, improving breastfeeding self-efficacy, and preventing breast complications during lactation are effective to increase exclusive breastfeeding practices.

Conclusions: Stress levels after breastfeeding, breastfeeding self-e cacy, and presence of breast complications could be modi able factors related to subsequent exclusive breastfeeding. Further research is needed to examine whether approaches to reducing breastfeeding-related stress, improving breastfeeding self-e cacy, and preventing breast complications during lactation are effective to increase exclusive breastfeeding practices.

Background
The World Health Organization recommends exclusive breastfeeding for at least 6 months after childbirth for optimal growth, development, and well-being of children [1]. However, in Japan, the rate of exclusive breastfeeding in the rst 3 months postpartum ranged from only 51 to 55% in 2015 [2]. According to a national survey in Japan [3], 41.7% of women planned exclusive breastfeeding during pregnancy, 49.3% stated that they would breastfeed if possible; that is, more than 90% expressed a desire to breastfeed. At 1 month postpartum, 67.6% of the women who planned exclusive breastfeeding, and 40.7% of those who stated that they would breastfeed if possible were exclusively breastfeeding. Although many pregnant women have a desire to breastfeed, actual postpartum feeding modality does not necessarily conform to antenatal intent.
Exclusive breastfeeding practice is related to demographic, physiological, and psychological factors. The demographic factors including age, parity, and education level have consistently characterized exclusive breastfeeding mothers [4][5][6]. Mothers who did not experience breast complications such as nipple pains reported practicing exclusive breastfeeding more than those with breast complications [7]. Such physiological barriers are likely to increase stress levels and cause women to discontinue breastfeeding sooner [8]. In addition, psychosocial factors, including breastfeeding-related self-e cacy, stress levels, and family support, might also predict exclusive breastfeeding practice. According to Otsuka et al. [9], low breastfeeding self-e cacy is associated with the perception of insu cient milk. This perception may lead to milk supplementation [3]. In a cross-sectional study, subjective child-related stress responses were reported to be higher in women who were partially breastfeeding than in those who were exclusively breastfeeding [10]. Meanwhile, an association between breastfeeding-related stress and subsequent breastfeeding practice has been not clari ed, although psychological stress decreases suckling-induced oxytocin release [11]. Kaneko et al. [12] reported that husband support, such as advice on child-rearing, is associated with exclusive breastfeeding. The effects of these physiological and psychosocial factors on subsequent exclusive breastfeeding practice have not been longitudinally examined.
To meet the breastfeeding expectations of women and promote exclusive breastfeeding practices, we aimed to examine the modi able factors at 1 month postpartum related to exclusive breastfeeding at 3 months postpartum. In particular, we focused on breastfeeding-related and psychosocial variables such as breast complications, breastfeeding self-e cacy, stress levels, depressive symptoms, bonding, and family support. Breastfeeding-related stress levels were assessed using salivary cortisol measurement,since objective stress markers can re ect immediate stress responses better than subjective assessment. A clearer understanding of these associations may help healthcare professionals develop important interventions to promote exclusive breastfeeding.

Participants and Setting
This prospective cohort study was a secondary analysis of a longitudinal study. The longitudinal study from the third trimester to 5 months postpartum was conducted in a secondary medical care center in Osaka, Japan from February 2017 to October 2018. The research hospital was not a baby-friendly hospital as de ned by the World Health Organization/United Nations International Children's Emergency Fund. Healthy Japanese women at 34-36 weeks' gestation who visited the hospital for medical checkup were recruited. The following women were excluded: those younger than 20 years old, those with inadequate Japanese literacy, and those with psychiatric diseases. All participants provided written informed consent prior to the baseline investigation. Of the investigation data available at the third trimester, a few days after childbirth, and 1, 3, and 5 months postpartum in the longitudinal study, we used the data from the third trimester and at 1 and 3 months postpartum. The investigations at 1 and 3 months postpartum were conducted by mail. We did not use the data at a few days postpartum since the breastfeeding-related stress levels in this period seemed to be unstable. This was because many women have breast complications, such as nipple pains and breast engorgement, and are not accustomed to the breastfeeding process. In addition, we did not use the data at 5 months postpartum because of the high dropout rate. We also used data on delivery outcomes from the participants' medical charts.

Variables
The original questionnaire distributed to the mothers at 34-36 weeks' gestation contained questions on age, parity, education level, height, and pre-pregnancy weight. After childbirth, we obtained information about delivery mode, blood loss during delivery, and infant's birth weight from the medical charts. At 1 month postpartum, we mailed a questionnaire and a box containing two tubes for saliva sampling and icepack to the participants. The participants collected 1.0-mL saliva samples twice (before and after breastfeeding of 11:00-15:00). Salivary cortisol levels were measured as an indicator of physiological and psychological responses associated with breastfeeding. The sampling time 11:00-15:00 was chosen because cortisol levels during this time are comparatively stable in the circadian rhythm. The participants were asked not to eat or drink in the 15 minutes before the saliva sampling. After the sampling, they packed the two saliva samples and the icepack into the box and mailed them to the research university using a frozen delivery service. Thereafter, the saliva samples were stored at −30°C until analysis. The sampling method used was that referred to in the study of Kusaka et al [13]. The salivary cortisol levels were measured using a Cortisol Salivary Immunoassay Kit (Salimetrics, LLC, CA, USA).
The questionnaire at 1 month postpartum contained questions on infant feeding modality, breast complications (nipple pains, cracked nipples, nipple shape, breast induration, and breast in ammation), the Japanese version of the Breastfeeding Self-E cacy Scale Short Form (BSES-SF) [9], the Japanese version of the Perceived Stress Scale-10 (PSS-10) [14], the Japanese version of the Edinburgh Postnatal Depression Scale (EPDS) [15], the Japanese version of the Postpartum Bonding Questionnaire (J-PBQ) [16], and support from husbands or parents. Infant feeding modality was selected from among exclusive breastfeeding, partial breastfeeding, or formula feeding.
The BSES-SF was developed to assess a person's belief and con dence in their ability to breastfeed [9,17]. The breastfeeding self-e cacy theoretical framework developed by Dennis [18] was based on Bandura's social cognitive theory [19]. This scale consists of 14 items that require ve-point Likert scale responses ranging from "not at all con dent" to "very con dent" (total, 14-70 points). Higher scores indicate a higher level of self-e cacy. Cronbach's α of the present study was 0.849.
The PSS-10 was used to assess the degree to which situations in one's life are appraised as stressful [14,20]. This scale consists of 10 items requiring ve-point Likert scale responses (total, 0-40 points). Higher scores indicate higher levels of stress. Cronbach's α of the present study was 0.854.
The EPDS assesses whether a person had depressive symptoms within the preceding 7 days [15,21]. This scale is a 10-item self-reported screening tool for perinatal depression with a total score between 0 and 30. In Japan, a postpartum woman with a score >8 points is considered to have depressive symptoms [15]. Cronbach's α of the present study was 0.792.
The J-PBQ, which consists of 14 items, was used to assess whether participants had bonding disorders [16]. The J-PBQ was developed based on the original PBQ by Brockington et al. [22], which consists of 25 items. The J-PBQ has six-point Likert scale responses ranging from "never" to "always" (total, 0-70 points). Higher scores indicate a greater bonding disorder. Cronbach's α of the present study was 0.813. At 3 months postpartum, we re-assessed each infant's feeding modality.

Statistical Analysis
Student's t-test, Mann-Whitney U test, Chi-square test, or Fisher's exact test was used to compare participant characteristics between women who were exclusively breastfeeding and those who were not, at 3 months postpartum. Multiple logistic regression analyses were performed to examine the factors related to exclusive breastfeeding at 3 months postpartum. Variables with p values < 0.10 for binary analyses and demographic variables (age, parity, and education level) that were detected as related factors to breastfeeding by previous studies [4,11] were entered as independent variables into the multiple logistic regression models. Independent variables in the regression nal model were determined using backward elimination (Wald). These analyses were conducted according to parity. All differences with a 2-sided p value < 0.05 were considered statistically signi cant. Statistical analyses were performed using Statistical Package for Social Sciences v. 24.0® (IBM Corp, Armonk, NY, USA).

Results
Of the 349 healthy women at 34-36 weeks' gestation who were asked to participate in the research, 269 provided written informed consent. Among them, 70 were excluded due to consent withdrawal by 1 month postpartum (n = 66), psychological condition due to after-effects of earthquake (n = 2), severe infant condition (n = 1), and isolation by infection (n = 1). Thus, we asked 199 (74.0%) women to answer questionnaires and collect saliva samples at 1 month postpartum. Forty-one women did not submit questionnaires and salivary samples. Of the 158 (58.7%) kits received, 43 were excluded due to incomplete data (n = 33), answering questionnaires over 60 days after childbirth (n = 5), inadequate salivary sampling (n = 4), and formula feeding (n = 1). At 3 months postpartum, we asked 115 (42.8%) women to answer a questionnaire about infant feeding modality. Eleven women did not return the questionnaire. A total of 104 (38.7%) women provided complete baseline data, answered further questionnaires, and provided daytime saliva samples. No differences in demographic variables, and infant feeding modality and salivary cortisol levels at 1 month postpartum were found between the dropouts and the participants who completed all of the investigations. Table 1 shows the summary of participant characteristics. Of the 104 women, 61 (58.7%) reported exclusive breastfeeding at 3 months postpartum; 33 (31.7%), partial breastfeeding; and 10 (9.6%), formula feeding. The analyses were conducted according to parity, since parity was strongly associated with breastfeeding practice and other variables.
The associations between breastfeeding-related and psychosocial variables at 1 month postpartum and exclusive breastfeeding at 3 months postpartum are shown in Table 2. Of the women who were not exclusively breastfeeding at 1 month postpartum, 14 (26.9%) changed to exclusive breastfeeding at 3 months postpartum. By contrast, 5 (10.4%) women who were exclusively breastfeeding at 1 month postpartum changed to partial breastfeeding by 3 months postpartum. Forty-ve (43.3%) women had higher salivary cortisol levels after breastfeeding compared to before.
On multiple logistic regression analysis (Table 3), the following factors signi cantly affected exclusive breastfeeding at 3 months postpartum: all participants (multiparity, having a university degree, no plan to return to work by 6 months postpartum, exclusive breastfeeding at 1 month postpartum, higher BSES-SF score at 1 month postpartum, and lower cortisol level after breastfeeding at 1 month postpartum); primiparas (exclusive breastfeeding and lower cortisol level after breastfeeding at 1 month postpartum); and multiparas (lower cortisol level after breastfeeding, higher BSES-SF score, and absence of breast complications at 1 month postpartum).

Discussion
Lower salivary cortisol levels after breastfeeding at 1 month postpartum were associated with exclusive breastfeeding at 3 months postpartum, regardless of parity. Furthermore, higher breastfeeding selfe cacy and absence of breast complications at 1 month postpartum were possible modi able predictors of exclusive breastfeeding at 3 months postpartum.
Lower cortisol levels after breastfeeding were associated with subsequent exclusive breastfeeding practices. Notably, the relationship was observed despite no cross-sectional relationship between cortisol levels and exclusive breastfeeding at 1 month postpartum. Cortisol levels usually decrease after breastfeeding since oxytocin inhibits cortisol secretion in women without mood distress [23]. Nevertheless, more than 40% of participants in the present study had increased cortisol levels after breastfeeding compared with before. High cortisol levels after breastfeeding despite oxytocin action seem to re ect physiological and psychological stress related to breastfeeding. Previous studies reported no relationship between perceived stress and milk volume, although oxytocin levels were decreased in women with psychological stress compared to those without [11,24]. Thus, it is assumed that breastfeeding-related stress affects subsequent exclusive breastfeeding practice through psychological burden and associated behavioral changes, not through fundamental physiological changes in lactation, such as milk volume reduction. A stress response after breastfeeding is a modi able factor. Approaches to stress reduction including preventing breast complications, relieving anxiety by providing advice about breastfeeding concerns, and relaxation during breastfeeding could be effective [25]. In addition, maternal cortisol responses to breastfeeding vary according to the function of the CD38 rs3796863 [26], an ectoenzyme that mediates the release of oxytocin. A recent study has indicated that the CD38 rs3796863 CC genotype is associated with a reduced release of oxytocin during breastfeeding and, accordingly, fewer cortisol-reducing responses to breastfeeding [27]. The speci c gene in uences the association between breastfeeding and its cortisol responses through reduced oxytocin secretion, not through breastfeeding-related psychological stress. Thus, an association between post-breastfeeding cortisol levels and subsequent breastfeeding might be attenuated by the analyses without considering the gene. Further studies are needed to clarify the associations.
A higher BSES-SF score was associated with subsequent exclusive breastfeeding as reported by a previous study of another population [28]. Breastfeeding self-e cacy re ects a mother's con dence in her ability to breastfeed her infant. The BSES-SF contains the following items "I can always keep wanting to breastfeed" and "I can always be satis ed with my breastfeeding experience" [9,17]. Women with positive answers to such items seemed less stressed about breastfeeding. Women with lower breastfeeding selfe cacy were also reportedly more likely to perceive milk insu ciency [9,29]. Such a perception has been described as a factor related to cessation of exclusive breastfeeding [30]. The perception of milk insu ciency itself was not assessed in our study because this concept was supposed to be contained in questions of the BSES-SF. A further detailed study regarding the relationship between breastfeeding selfe cacy, perception of milk insu ciency, and subsequent exclusive breastfeeding may contribute to the suggestion of concrete intervention methods for increasing the rate of exclusive breastfeeding. In the analyses according to parity, the association between breastfeeding self-e cacy and exclusive breastfeeding was observed only in multiparas. A previous study showed that the effect of self-e cacy on breastfeeding practice was much stronger in multiparas than primiparas [31]. This was because breastfeeding experiences in primiparas were affected more by subjective norms and social environment than breastfeeding self-e cacy [31]. Therefore, the effectiveness of improving breastfeeding self-e cacy on breastfeeding practices may differ according to parity. A systematic review showed that prenatal and postpartum interventions focusing on improving breastfeeding self-e cacy lead to exclusive breastfeeding [32]. However, in Japan, the effects of prenatal intervention using a breastfeeding selfe cacy workbook are limited and effective in only baby-friendly hospitals and in the early postpartum period [33]. Development of more effective approaches taking parity into consideration are needed for postpartum Japanese women.
In multiparas, absence of breast complications at 1 month postpartum was associated with subsequent exclusive breastfeeding. Although this association supported previous studies [34,35], we did not ascertain the reason why it was observed only in multiparas. In general, primiparas experienced more breast complications than multiparas [36], as observed in the present study. Furthermore, breast complications strongly relate to psychological breastfeeding-related stress [37]. The strength of the association between the presence of breast complications, breastfeeding-related stress, and exclusive breastfeeding practice may depend on participant characteristics and individual stress responses associated with breast complications. However, educational intervention for prevention of breast complications is essential to relieve breastfeeding-related stress and increase exclusive breastfeeding practices.
As with previous studies, parity and education level were associated with exclusive breastfeeding [4,12]. However, the effect of parity on exclusive breastfeeding practice is not a simple correlation; rather, it often varies by study populations and previous breastfeeding experiences in multiparous women [5,38,39]. Women with higher education levels easily access health-related information and have more favorable attitudes toward breastfeeding [40,41]. Such behavioral characteristics in women with higher education levels might help them achieve exclusive breastfeeding.
Returning to work by 6 months postpartum was associated with less exclusive breastfeeding at 3 months postpartum. Postpartum women who planned to return to work in the earlier postpartum period tended to select partial breastfeeding or formula feeding [29,42]. In Japan, continuing exclusive breastfeeding is di cult for some working women because of the work environment and nursery policies. A private space and consideration for expressing breast milk during working hours are often lacking, although many companies have been attempting to provide such environments. Nursery policies often refuse breast milk storage due to hygienic reasons. Such situations sometimes make women discontinue exclusive breastfeeding [43]. In addition, partners' attitudes against breastfeeding and childcare could be important elements that prevent women from discontinuing breastfeeding after returning to work [44].
Environmental and emotional support from family members, employers, and nursery staff members may be essential for working women to continue exclusive breastfeeding.
Exclusive breastfeeding at 1 month postpartum is a strong predictor of the same at 3 months postpartum. However, even if women are not exclusively breastfeeding at 1 month postpartum, they may change to exclusive breastfeeding as observed in the present study. The rst 3 months after childbirth remain a critical period for the establishment of exclusive breastfeeding [45]. Thus, medical and psychological approaches in this period would be signi cant. Stress levels after breastfeeding, breastfeeding self-e cacy, and breast complications are possible key modi able predictors. In Japan, women have state-funded medical checkups at 1 month postpartum. Thereafter, if they desire medical care regarding breastfeeding, they have to access it by themselves. By 1 month postpartum, healthcare providers' advice and intervention for reducing breastfeeding-related stress responses, improving breastfeeding self-e cacy, and preventing breast complications may be effective in establishing and continuing exclusive breastfeeding. Further intervention studies are required to con rm the effectiveness.
The present study had two limitations. First, the dropout rate was higher than expected. Although no differences in infant feeding modality and salivary cortisol levels between dropouts and participants were found, the high dropout rate may have affected the relationship between cortisol levels and breastfeeding practice. Second, we could not follow the participants for a full 6 months postpartum, although exclusive breastfeeding for 6 months is recommended. However, the key strength of this study is that we showed the relationship between stress responses associated with breastfeeding and subsequent exclusive breastfeeding, using objective measures of stress.

Conclusions
Breastfeeding-related stress levels at 1 month postpartum were identi ed as a possible modi able predictor of exclusive breastfeeding at 3 months postpartum, regardless of parity. In multiparas, breastfeeding self-e cacy and presence of breast complications at 1 month postpartum could also be possible modi able factors. Further research is needed to determine whether approaches to reducing breastfeeding-related stress, improving breastfeeding self-e cacy, and preventing breast complications are effective in increasing exclusive breastfeeding practices.