Abstract
Aims
The aims of the present study were to examine the association between late pregnancy exposure to serotonin reuptake inhibitor (SRI) antidepressants and difficulties in achieving an adequate breast milk supply in women who have given birth to preterm infants, while accounting for the potential impacts of underlying maternal psychiatric illness.
Methods
A retrospective cohort study was carried out of 3024 women delivering liveborn preterm infants (<37 weeks' gestation) between January 2004 and December 2008. The primary outcome was postnatal domperidone use, considered to be a valid proxy for the presence and pharmacological management of low milk supply. Relative risks adjusted for maternal sociodemographic characteristics and comorbidities (aRRs) were calculated for low milk supply, comparing women with late pregnancy exposure to SRI antidepressants (n = 86), women with a psychiatric illness but no antidepressant use (n = 126) and women with neither antenatal exposures (n = 2812).
Results
Compared with non‐exposed women, nonmedicated psychiatric illness [aRR 1.64; 95% confidence interval (CI) 1.16, 2.30] but not late pregnancy SRI use (aRR 1.00; 95% CI 0.59, 1.70) was associated with an increased risk of domperidone use, indicative of low milk supply.
Conclusions
These findings do not support the previously observed negative impacts of antidepressant use on breastfeeding, instead suggesting that women with an underlying psychiatric illness appear at greatest risk of experiencing low milk supply and could benefit from additional breastfeeding education and support.
Keywords: antidepressive agents, breastfeeding, lactation, premature birth, serotonin agents
What is Already Known about this Subject
Serotonin plays an important role in human breast milk volume homeostasis within the mammary gland during lactation.
Previous research has demonstrated that women taking antidepressants have lower rates of breastfeeding intention and initiation, and are more likely to experience delayed secretory activation.
It is unclear whether the use of serotonin reuptake inhibitors (SRIs) during lactation is associated with a reduction in breast milk volume or leads to impaired long‐term breastfeeding outcomes.
What this Study Adds
In a cohort of mothers of preterm infants, use of SRIs in late pregnancy was not associated with an increased risk of experiencing low milk supply.
Women with an underlying psychiatric illness appeared at greatest risk of experiencing low milk supply and could therefore benefit from additional breastfeeding education and support.
Introduction
http://www.guidetopharmacology.org/GRAC/LigandDisplayForward?ligandId=5 has been identified as playing an important role in human breast milk volume homeostasis within the mammary gland during lactation, with increased levels leading to mammary gland involution and reduced milk production 1. This raises concerns that medications that alter serotonin signalling, such as the serotonin reuptake inhibitor (SRI) antidepressants, may interfere with the normal physiological processes involved in lactation and therefore place women at increased risk of poor breastfeeding outcomes. Previous research has identified that women taking antidepressants have lower rates of breastfeeding intention and initiation 2, 3, but most recent evidence suggests this is largely due to residual confounding from underlying maternal psychiatric illness 4. However, Marshall et al. demonstrated an association between maternal selective serotonin reuptake inhibitor (SSRI) use and delayed secretory activation (defined as onset of copious milk production; also known as stage II lactogenesis) which was independent of underlying maternal depressive illness 5. While it is well established that delayed secretory activation is associated with a reduced duration of breastfeeding 6, it is unclear whether this observed delay associated with SSRI use is also associated with a reduction in breast milk volume or leads to impaired long‐term breastfeeding outcomes. Therefore, the aim of the present study was to examine the association between late pregnancy exposure to SRIs and difficulties in achieving an adequate breast milk supply in women who have given birth to preterm infants, while accounting for the potential impacts of underlying maternal psychiatric illness.
Methods
Study design and setting
We conducted a retrospective cohort study of all women delivering liveborn preterm infants (<37 weeks' gestation) at the Women's and Children's Hospital (WCH) in South Australia between January 2004 and December 2008 (n = 3054). We excluded women exposed to antidepressants other than SRIs (n = 13) or antipsychotic agents (n = 17), leaving a final cohort of 3024 women.
The WCH is accredited as part of the Baby Friendly Hospital Initiative (BFHI) and has a dedicated lactation support service. This study utilized linkable electronic health administrative data within the WCH, including the WCH perinatal statistics collection (PSC) and the WCH hospital pharmacy dispensing records. The PSC includes electronic data on the pregnancy and outcome of every live birth and late fetal death occurring at the hospital 7. The information in the PSC has been previously validated and is reliable when compared with hospital case records 8. These data have been previously utilized to investigate outcomes associated with the use of antidepressants during pregnancy and the use of domperidone for the management of low milk supply, the full details of which have been published previously elsewhere 9, 10.
Measures
Antidepressant use and psychiatric illness
Late pregnancy exposure to SRIs was identified from the WCH pharmacy dispensing records. Women were classified as exposed if they had been dispensed an SRI antidepressant during late pregnancy (second and third trimesters). Hospital pharmacy dispensing records have previously been validated as an indicator of exposure to antidepressants in late pregnancy, including exposure around the time of delivery 7. In an effort to obtain a suitable comparison group consisting of women with similar underlying disease to those exposed to antidepressants during pregnancy, we identified a cohort of women with an identified psychiatric illness during pregnancy but who had not been dispensed an antidepressant (disease comparison termed ‘nonmedicated psychiatric illness’). The presence of a psychiatric illness during pregnancy was identified from the electronic PSC, with midwives recording the diagnosis if the woman was receiving medication for her psychiatric illness or if it was recorded in the notes that the woman had received psychological/psychiatric support during her pregnancy. This has been utilized as a disease comparator group in previous studies 11. The remaining group of women consisted of those who did not have a psychiatric illness and had not been dispensed an antidepressant (termed ‘non‐exposed’).
Breastfeeding outcomes and domperidone use
The primary outcome was postnatal domperidone use. Domperidone is a galactagogue which stimulates and promotes milk production and is commonly used as a pharmacological treatment for mothers who are experiencing lactation difficulties 12, 13. Therefore, domperidone use was considered to be a proxy for the presence and pharmacological management of low milk supply. Data relating to women who had been dispensed domperidone were obtained from the WCH pharmacy dispensing records, in accordance with previously published methods 9. Domperidone can only be prescribed by medical doctors for mothers of preterm infants in the neonatal unit, utilizing a preprinted prescribing checklist, with no restrictions according to level of experience (e.g. interns, registrars and consultants are all eligible to prescribe). Prescribers in the neonatal unit are only allowed to prescribe mothers domperidone for the explicit indication of lactation insufficiency, with mothers referred to other physicians for the management of conditions not affecting their infant. We have previously undertaken a detailed medication chart review for a random selection of 215 of 1605 mother–infant dyads where domperidone was prescribed, with 100% of records indicating that domperidone was prescribed for lactation insufficiency 9. Guidelines regarding the use of domperidone for the management of low milk supply during this period have remained consistent, recommending domperidone as the first‐line pharmacological treatment. Domperidone is the most widely prescribed first‐line agent for the management of maternal low milk supply across Australian neonatal units 13. Data on any breastfeeding at neonate discharge from hospital are collected routinely and were utilized to determine additional breastfeeding outcomes. Furthermore, in the 2008 calendar year only, additional data were also available pertaining to initiation of breastfeeding and exclusivity of breastfeeding during infant admission to the neonatal unit.
Covariates
Data on additional maternal and neonatal characteristics were obtained from the PSC. Maternal age and body mass index (BMI) were determined at the time of first antenatal booking visit. Women were classified as nonsmokers or smokers during pregnancy, based on maternal self‐report at the first antenatal visit. The estimated length of gestational age at delivery was based on the last menstrual period and ultrasound examination. According to parity, women were classified as either primiparous or multiparous. The method of delivery was classified as either vaginal (including instrumental deliveries) or lower‐segment caesarean section (including elective and emergency). Maternal ethnicity was classified as Caucasian or other. Socioeconomic status for each woman was determined using her residential postcode at the time of delivery. Women were then ranked according to their level of advantage or relative disadvantage, based on data from the Socio‐Economic Indexes for Areas (SEIFA), calculated from the Australian Bureau of Statistics' 5‐yearly Census of Population and Housing. SEIFA scores were converted to quintiles, representing widely used measures of relative socioeconomic status.
Data analyses
The association between maternal SRI exposure status and domperidone use was evaluated using a generalized linear model (Poisson distribution) with robust variance estimates [and resulting relative risks (RRs) and 95% confidence intervals (CIs)]. Analyses were adjusted for possible confounders, including maternal age, parity, smoking status, socioeconomic status and gestational age at birth. We also conducted a sensitivity analysis restricting the analysis to the 2008 calendar year, when data on breastfeeding initiation and exclusivity of breastfeeding during infant's neonatal unit admission were available. Statistical significance was defined as a two‐sided P‐value of <0.05. All statistical analyses were undertaken using STATA IC 14 (Stata, College Station, TX, USA).
Ethical approval
The project was approved by the Women's and Children's Health Network Human Research Ethics Committee (REC2219–10‐14).
Nomenclature of targets and ligands
Key protein targets and ligands in this article are hyperlinked to corresponding entries in http://www.guidetopharmacology.org, the common portal for data from the IUPHAR/BPS Guide to PHARMACOLOGY 14.
Results
Among the cohort of 3024 eligible women, 86 (2.8%) were exposed to an SRI in late pregnancy, 126 (4.2%) were exposed to nonmedicated psychiatric illness and the remaining 2812 (93.0%) were non‐exposed.
Table 1 presents the demographic and clinical characteristics of women according to exposure status. While women exposed to SRIs in late pregnancy differed from non‐exposed women across a number of characteristics, they were largely representative of women with nonmedicated psychiatric illness.
Table 1.
Demographic and clinical characteristics for mothers of preterm infants exposed to serotonin reuptake inhibitors (SRIs), nonmedicated psychiatric illness or neither during late pregnancy
| Characteristic | SRI use (n = 86) | Nonmedicated psychiatric illness (n = 126) | Non‐exposed (n = 2812) |
|---|---|---|---|
| Age, mean ± SD | 30.2 (5.3) | 29.0 (6.2) | 29.5 (6.2) |
| Maternal BMI (kg m –2 ), mean ± SD | 26.9 (6.1) | 26.6 (6.8) | 26.3 (6.6) |
| Parity | |||
| Multiparous, n (%) a | 50 (58.1) | 71 (56.4) | 1441 (51.4) |
| Smoking status, n (%) a | |||
| Nonsmoker | 52 (61.9) | 68 (56.7) | 1889 (74.2) |
| Quit during pregnancy | 2 (2.4) | 7 (5.8) | 95 (3.7) |
| Smoker | 30 (35.7) | 45 (37.5) | 562 (22.1) |
| Ethnicity, n (%) a | |||
| Caucasian | 82 (95.4) | 116 (92.1) | 2289 (81.4) |
| Other | 4 (4.7) | 10 (7.9) | 523 (18.6) |
| Socioeconomic status, SEIFA, n (%) a | |||
| 5 (highest) | 11 (12.8) | 21 (16.7) | 441 (15.8) |
| 4 | 10 (11.6) | 25 (19.8) | 483 (17.3) |
| 3 | 15 (17.4) | 19 (15.1) | 478 (17.1) |
| 2 | 16 (18.6) | 21 (16.7) | 665 (23.8) |
| 1 (lowest) | 34 (39.5) | 40 (31.8) | 732 (26.2) |
| Psychotropic medication use, n (%) a | 6 (7.0) | 10 (7.9) | 50 (1.8) |
| Substance abuse, n (%) a | 6 (7.0) | 19 (15.1) | 144 (5.1) |
| Delivery type | |||
| Caesarean section | 50 (58.1) | 67 (53.2) | 1424 (50.6) |
| Gestational age (weeks), median (range) | 35 (25–36) | 34 (22–36) | 34 (23–36) |
| Dispensed domperidone, n (%) a | 14 (16.3) | 30 (23.8) | 410 (14.6) |
| Any breastfeeding at neonatal discharge from hospital, n (%) a | 74 (86.1) | 105 (84.0) | 2379 (84.8) |
| 2008 cohort only (n = 603) | |||
| Initiated breastfeeding, n (%) a | 19 (95.0) | 12 (85.7) | 499 (88.3) |
| Exclusively breastfed infant during entire neonatal unit admission, n (%) a | 4 (20.0) | 1 (7.1) | 115 (20.4) |
BMI, body mass index; SD, standard deviation; SEIFA, Socio‐Economic Indexes for Areas
Percentages are calculated from non‐missing data
The prevalence of domperidone use was highest among women with nonmedicated psychiatric illness (23.8%), followed by those with SRI use (16.3%) and those who were non‐exposed (14.6%). The unadjusted and adjusted differences in domperidone use between groups are presented in Table 2. Compared with non‐exposed women, nonmedicated psychiatric illness [adjusted RR (aRR) 1.64; 95% CI 1.16, 2.30) but not late pregnancy SRI use (aRR 1.00; 95% CI 0.59, 1.70) was associated with an increased use of domperidone use, indicative of low milk supply.
Table 2.
Multivariate analysis of postnatal domperidone use according to maternal late pregnancy exposure status
| SRI use vs. non‐exposed | SRI use vs. nonmedicated psychiatric illness | Nonmedicated psychiatric illness vs. non‐exposed |
|---|---|---|
| Unadjusted RR (95% CI) | ||
| 1.12 (0.66, 1.87) | 0.68 (0.37, 1.25) | 1.63 (1.17, 2.28) |
| Adjusted RR (95% CI) a | ||
| 1.00 (0.59, 1.70) | 0.62 (0.33, 1.16) | 1.64 (1.16, 2.30) |
CI, confidence interval; RR, relative risk; SRI, serotonin reuptake inhibitor
RR adjusted for maternal age, parity, smoking status, socioeconomic status and gestational age at birth
The cumulative percentage of women dispensed domperidone postpartum according to late pregnancy exposure status is presented in Figure 1. Across all groups, more than 50% of women who received domperidone were dispensed it within the first 3 weeks postpartum. The rate of domperidone use appeared similar among the SRI use and nonmedicated psychiatric illness groups within the first 3 weeks postpartum, before tapering off in the SRI use group while continuing to increase in the nonmedicated psychiatric illness group. Figure 2 demonstrates that the prevalence of domperidone use was highest among mothers with a nonmedicated psychiatric illness across all gestations.
Figure 1.
Cumulative percentage of women dispensed domperidone postpartum according to late pregnancy exposure status. SRI, serotonin reuptake inhibitor
Figure 2.
Percentage of women prescribed domperidone according to exposure status and gestational age at birth. SRI, serotonin reuptake inhibitor
In a sensitivity analysis involving only those women who delivered in the 2008 calendar year where data were available on breastfeeding initiation and we were able to restrict the cohort to women who initiated breastfeeding, no difference in domperidone use was observed between women with SRI use in late pregnancy and nonmedicated psychiatric illness (RR 1.05; 95% CI 0.28, 3.94). When further restricted to primiparous women, no difference in domperidone use was observed between women with SRI use in late pregnancy and nonmedicated psychiatric illness (RR 1.06; 95% CI 0.49, 2.28).
Discussion
Main findings
We found that use of SRIs in late pregnancy is not associated with an increased risk of domperidone use in mothers of preterm infants. These findings suggest that use of serotonin‐disrupting antidepressants during lactation does not place women at increased risk of experiencing low milk supply.
Strengths and limitations
To our knowledge, this is the largest study undertaken to investigate the potential impacts of maternal SRI use and nonmedicated psychiatric illness on breast milk supply difficulties. The major strength of the study lies in the identification of a group of women with nonmedicated psychiatric illness, providing greater adjustment for potential confounding associated with underlying maternal illness. Further, utilization of data on domperidone use as a proxy for the presence of low milk supply represents a novel approach towards addressing a topic of particular significant importance, with a previous clinical audit finding 100% agreement between domperidone use and management of lactation insufficiency. In accordance with hospital policy, domperidone is supplied to mothers in the neonatal unit utilizing a carefully developed prescribing checklist which requires prescriber acknowledgement of persistent low milk supply, despite previous utilization of nonpharmacological interventions. Therefore, domperidone supply is likely to represent those women experiencing the greatest breastfeeding difficulties. Further strengths of the present study include undertaking additional sensitivity analyses to determine the potential impact of breastfeeding initiation on observed breastfeeding outcomes.
There are a number of limitations associated with the study. Use of hospital pharmacy dispensing data may not have identified all women who were taking an antidepressant in late pregnancy, meaning that some women in the control groups may have been exposed to SRIs unknowingly. Such misclassification, however, is likely to be nondifferential with respect to the outcome under investigation and therefore is unlikely to have had a large impact on the effect estimate 15. We are not able to confirm that women exposed to an SRI in late pregnancy continued to take it while breastfeeding and we do not have data on whether women in the nonmedicated psychiatric illness or non‐exposed group were prescribed an antidepressant in the postpartum period. However, based on previous drug utilization studies 16, the number of women in the nonmedicated psychiatric illness group who may have been on an antidepressant previously and then restarted it during lactation is likely to be low, as is the relative number of women in the non‐exposed group who may have been newly prescribed an antidepressant in the postpartum period. In addition, there was no measure of the type and severity of maternal psychiatric illness, which would have added to our understanding of the independent effects of psychiatric illness on the risk of low milk supply, and we did not assess the impact of dose or indication of SRI use. A noteworthy limitation is that women identified as having a nonmedicated psychiatric illness (which excluded users of non‐SSRI antidepressant or antipsychotic agents) reflect a heterogeneous group with a range of likely psychiatric diagnoses and severities reflecting imbalances of other neurotransmitters, besides serotonin. Lastly, given that we restricted the study to mothers of preterm infants, it is unclear whether the findings will also be generalizable to mothers of term infants.
Interpretation
The role of serotonin and serotonin transport in the regulation of lactation has been reviewed in detail elsewhere 17. In brief, numerous animal studies have established serotonergic transmission as a key regulator of lactation homeostasis, with increased levels of serotonergic activity (including through use of SRIs) accelerating the rate of mammary gland involution, leading to a reduction in milk production 17. Whether similar effects occur in humans is unclear, as it has been previously noted that the mammary glands of mice, cattle and humans express unique patterns of serotonin receptors that vary among the species 18. The potential impacts of SRI exposure have been investigated in only one human study, where maternal SSRI use was associated with a twofold delay in secretory activation 5. Inconsistencies between the results of our study and those of other studies might be explained by a few noteworthy differences in methodology. The findings of Marshall et al. 5 were based on a sample of only eight mothers of term infants exposed to SSRIs, compared with our sample of 86 women taking SRIs. Furthermore, all women in the former study had experienced secretory activation by day 7, with no examination of breast milk volume or longer‐term breastfeeding outcomes 5. We focused on mothers of preterm infants as this was envisaged to enable us to obtain more complete data on domperidone use occurring within the hospital, and the longer neonatal hospital admission enabled examination of longer‐term breastfeeding outcomes. Further, mothers of preterm infants are the most vulnerable for experiencing difficulties with milk supply, and their infants benefit the most from the availability of the mother's milk for feeding. Given the additional breastfeeding support often available to mothers of preterm infants, it is possible that these may overcome any challenges related to delayed secretory activation and therefore avoid potential negative impacts posed by serotonin disruption during lactation.
Notably, these findings do not provide evidence against a role of serotonin in lactation; rather, they provide evidence that interference in serotonin signalling through antidepressant use is unlikely to have a direct impact on breast milk production. It is well recognized that successful lactation is moderated by a range of behavioural, social, clinical and biological factors, with one of the most significant clinical factors being giving birth to a preterm infant 19. Of note, previous studies have demonstrated that acute and chronic physical and mental stress can impair the milk ejection reflex by attenuating oxytocin release 19. This could lead to incomplete emptying of the breast and a resultant reduction in overall milk production. This may explain why underlying maternal psychiatric illness appeared to have the greatest impact on inadequate breast milk supply, and point toward the need for increased awareness of maternal illnesses that can affect milk supply, to identify women who may require additional support and education to attain optimal breastfeeding outcomes. These findings suggest the need to provide additional attention and support to women taking antidepressants during lactation. Although the risks to the breastfed infant associated with antidepressant use in lactation are considered low, the choice to breastfeed when taking an antidepressant may pose a dilemma for some women 20. Concerns regarding infant ‘exposure’ through human milk may lead to unnecessary anxiety among mothers, and in turn have a negative impact on the physiological processes involved in lactation or their determination to persist with breastfeeding in spite of any difficulties that arise.
In conclusion, we found no evidence that use of SRIs in late pregnancy was associated with an increased risk of low milk supply in mothers of preterm infants. Women with an underlying psychiatric illness appear to be at greatest risk of experiencing low milk supply and could therefore benefit from additional breastfeeding education and support.
Competing Interests
All authors have completed the Unified Competing Interest form at http://www.icmje.org/coi_disclosure.pdf (available on request from the corresponding author) and declare: no support from any organization for the submitted work; no financial relationships with any organizations that might have an interest in the submitted work in the previous 3 years; no other relationships or activities that could appear to have influenced the submitted work.
The authors wish to acknowledge the assistance provided by Ann Fitzgerald, Manager of Clinical Information Services at the Women's and Children's Hospital. L.E.G. and L.H.A. receive salary support in the form of fellowships provided by the Australian National Health and Medical Research Council (NHMRC). Specific project funding support was provided by a Women's and Children's Hospital Research Foundation, 2013 MS McLeod Departmental Research Grant. The study sponsors had no involvement in the collection, analysis and interpretation of data, or in writing the manuscript.
Contributors
L.E.G. conceptualized and designed the study, carried out the initial analyses and drafted the initial manuscript. C.L., L.C., C.T.R. and L.H.A. helped to design the study, assisted in the interpretation of the results, and reviewed and revised the initial manuscript. All authors approved the final manuscript as submitted.
Grzeskowiak, L. E. , Leggett, C. , Costi, L. , Roberts, C. T. , and Amir, L. H. (2018) Impact of serotonin reuptake inhibitor use on breast milk supply in mothers of preterm infants: a retrospective cohort study. Br J Clin Pharmacol, 84: 1373–1379. doi: 10.1111/bcp.13575.
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