Assessing factors associated with poor maternal mental health among mothers of children born small and sick at 24–47 months in rural Rwanda

Background Global investments in neonatal survival have resulted in a growing number of children with morbidities surviving and requiring ongoing care. Little is known about the caregivers of these children in low- and middle-income countries, including maternal mental health which can further negatively impact child health and development outcomes. We aimed to assess the prevalence and factors associated with poor maternal mental health in mothers of children born preterm, low birthweight (LBW), and with hypoxic ischemic encephalopathy (HIE) at 24–47 months of age in rural Rwanda. Methods Cross-sectional study of children 24–47 months born preterm, LBW, or with HIE, and their mothers discharged from the Neonatal Care Unit (NCU) at Kirehe Hospital between May 2015–April 2016 or discharged and enrolled in a NCU follow-up program from May 2016–November 2017. Households were interviewed between October 2018 and June 2019. Mothers reported on their mental health and their child’s development; children’s anthropometrics were measured directly. Backwards stepwise procedures were used to assess factors associated with poor maternal mental health using logistic regression. Results Of 287 total children, 189 (65.9%) were born preterm/LBW and 34.1% had HIE and 213 (74.2%) screened positive for potential caregiver-reported disability. Half (n = 148, 51.6%) of mothers reported poor mental health. In the final model, poor maternal mental health was significantly associated with use of violent discipline (Odds Ratio [OR] 2.29, 95% Confidence Interval [CI] 1.17,4.45) and having a child with caregiver-reported disability (OR 2.96, 95% CI 1.55, 5.67). Greater household food security (OR 0.80, 95% CI 0.70–0.92) and being married (OR = 0.12, 95% CI 0.04–0.36) or living together as if married (OR = 0.13, 95% CI 0.05, 0.37) reduced the odds of poor mental health. Conclusions Half of mothers of children born preterm, LBW and with HIE had poor mental health indicating a need for interventions to identify and address maternal mental health in this population. Mother’s poor mental health was also associated with negative parenting practices. Specific interventions targeting mothers of children with disabilities, single mothers, and food insecure households could be additionally beneficial given their strong association with poor maternal mental health.


Background
Globally, over 20 million children are born at low birthweight (LBW < 2500 g) each year, nearly 15 million children are born preterm (gestational age < 37 weeks), 32 million infants are born small for their gestational age, and 1 million newborns have neonatal encephalopathy due to birth complications [1][2][3][4]. A third of neonatal deaths are due to complications of prematurity and a quarter are due to intrapartum complications such as birth asphyxia which leads to hypoxic ischemic encephalopathy (HIE) [5]. Children born preterm, LBW or with HIE and other medical vulnerabilities also have an increased risk for poor physical and psychosocial developmental outcomes [6,7]. In turn, mothers of these children are vulnerable to psychological distress from caring responsibilities and ongoing challenges such as poor growth that many of these children may experience [8][9][10][11]. Studies that compared parenting stress between mothers of preterm and term babies revealed that having a preterm child is associated with high levels of depressive symptoms and stress [9,[12][13][14].
Understanding the burden of poor mental health on mothers of children born small and sick is essential to inform interventions that promote the well-being of parents and better developmental outcomes of their children. While effects of maternal stress and preterm birth outcomes may vary by context, poor caregiver's mental health is associated with poor infant growth and cognitive development [13,[15][16][17][18][19]. However, treatment approaches based on increasing social support and enhancing mother-infant interactions have been proven effective to improve maternal mental health status and simultaneously improve child developmental status [10,20].
Despite the effectiveness of treatment, in most lowand middle-income countries, maternal mental health services have not been incorporated into the primary health care system [21], and 76-85% patients with mental health problems do not receive any intervention [19]. In Africa and Asia, the prevalence of maternal depression is estimated at 15-28% [10]. Additionally, in a postconflict country, such as Rwanda, there is an increased likelihood of maternal distress disorders [22] which may be further exacerbated in cases of prematurity, LBW and HIE. Poor maternal mental health has been identified among caregivers of children born small or with HIE in high-income countries, in part due to the stresses of uncertain survival and potential ongoing impairment among children with these conditions [23,24]. However, despite some small studies identifying a high prevalence of maternal depression and anxiety in areas of Rwanda [25,26], the country's decentralized mental health services are focused on more severe mental illnesses, such as schizophrenia [27]. Like many other low-and middleincome countries there are no specific interventions for maternal depressive symptoms and anxiety [28]. Thus, maternal depression and other distress disorders which are frequently complicated by social, emotional, and financial difficulties [29], go unaddressed. The existing evidence suggests that interventions to improve maternal mental health would also contribute to reducing the burden of childhood undernutrition so would be mutually beneficial to mother and child [30].
Rwanda has made efforts in improving outcomes for children in early childhood through improved health services at health facilities, community-based interventions for children under 5 years including community case management and community nutritional screening, as well as a growing priority on promoting optimal early childhood development [31,32]. In Rwanda, 10% of newborns are born preterm each year and 7% are born with LBW [33]. Prematurity/LBW and HIE are two of the three leading causes of admission to hospital neonatal care units in Rwanda [34]. However, to our knowledge, mental health among mothers of children with these perinatal risk factors has not been studied in Rwanda. Therefore, this study aims to assess the prevalence and factors associated with poor maternal mental health among mothers of children born preterm, LBW or with HIE when the children are ages 24-47 months.

Study setting
This study was conducted in Kirehe District in the Eastern Province of Rwanda. Kirehe District is served by Kirehe District Hospital (KDH), which is operated by the  [37].

Study design and population
This was a cross-sectional study that included children aged 24-47 months born with prematurity, LBW, or HIE, and discharged from the NCU at Kirehe District Hospital between May 2015 and April 2016 or enrolled in the PDC from May 2016 to November 2017. Primary caregivers of these children were included in this study if they were the biological mothers and if data on their mental health status was collected.

Data collection
Data were collected between October 2018 and June 2019 by a trained team of Partners In Health/Inshuti Mu Buzima data collectors. Data collectors conducted household interviews in Kinyarwanda with primary caregivers of eligible children, and measured anthropometrics and developmental indicators for children. Due to limitations in literacy, the data collector conducted the consent process and interview verbally and written confirmation of consent was provided by participants with a signature or fingerprint. The collected data included caregiver-reported child's developmental status, child's caregiver-reported disability status, child feeding, caregiver mental health, household socio-economic status, child discipline practices, and early stimulation activities. The child's nutritional status was measured directly.

Measures
Primary outcome Maternal mental health was measured using the Hopkins Symptom Checklist, which has been validated in Rwanda. It is a 25 item measure of symptoms of anxiety and depression with the total score being a mean of all items; a score > 1.75 is considered high level of anxiety and depression symptoms [38]. The full questionnaire is available in Supplementary File 1.
Covariates Stunting (low height-for-age), wasting (low weight-for-height), and underweight (low weight-forage) were measured using standard anthropometric procedures to capture weight and height (or length) and compared to the WHO Child Growth Standards [39]. The cutoff point for severe malnutrition was a z-score less than − 3 standard deviations and moderate malnutrition is a z-score less than − 2 standard deviations using the WHO Child Growth Standards.
Home environment was assessed using UNICEF's Family Care Indicators [40], which measure early learning activities, availability of play materials, and exposure to inadequate care. Inadequate care is when caregivers reported that the child was left alone, or the child was cared for by another child less than 10 years of age, for 1 hour or more in the past week. The UNICEF Multiple Indicator Cluster Survey measure of violent discipline [41] was also used. Exposure to violent discipline was defined as caregiver-reported use of any psychological aggression (i.e., yelling, name calling) or physical punishment (i.e., hitting, spanking) to the child in the past month.
Household socioeconomic status was measured using an asset index which was analyzed using principal component analysis for a measure of relative wealth in our sample; households were grouped into tertiles representing the poorest, the middle, and the wealthiest groups. In addition, the Rwandan "Ubudehe" categorization was collected, which is a Rwandan community-based ranking of wealth status. Households are categorized in to 4 groups with the first category being the extremely poor and qualifying for government social services including free health insurance, and the fourth being the wealthiest category.
Child disability was measured using the Ten Questions Questionnaire [42], which is a caregiver-reported screening tool for detecting impairments in physical development, hearing, vision, and communication. Children whose mother responded to yes on any one impairment were considered at risk for moderate to severe disability.
Child development was measured using the Ages and Stages Questionnaire (ASQ-3) [43]. The ASQ-3 asks 30 age-specific questions across communication, gross motor, fine motor, personal social, and problem solving domains. Children are screened as "at risk for developmental delay" if they fall below the standard Westernnormed cut-point in any one of the five domains.
Social support was measured using the Inventory of Socially Supportive Behaviors which had been previously adapted to Rwanda and is scored as a mean score of all items with 1 being the minimum score (low social support) and 5 being the maximum [44,45].
Months of Adequate Household Food Provisioning is a way to measure self-reported household food access over the past year [46].

Data analysis
We described socio-economic and demographic characteristics, child nutrition and development, home environment and maternal mental health using frequencies and percentages for categorical variables and mean and standard deviation (SD) or median and interquartile range (IQR) for continuous variables. Bivariate associations between maternal mental health status and each covariate was assessed using Fisher's exact (categorical) and t-test (continuous) or Wilcoxon rank sum test if continuous measures were not normally distributed (social support, months of adequate household food provisioning). Backwards stepwise techniques were used to build a multivariable logistic regression model to investigate factors associated with poor maternal mental health. We included in the full model all variables associated with maternal mental health at α = 0.20 in the bivariate analysis. Manual removal of variables was completed following backwards stepwise procedures and the final model included only variables significant at α = 0.05.
Factors associated with increased odds of poor maternal mental health in the final model included caregiverreported child disability (

Discussion
In this study, we found a high burden of poor maternal mental health (51.6%) among mothers with children born preterm, LBW and/or with HIE when the children were ages 24-47 months. This poor mental health was significantly associated with having a child with a caregiver-reported disability, single marital status, food insecurity in the household, and poor child discipline practices.
While the prevalence of poor maternal mental health in the population of Rwanda is unknown, we found about double the prevalence of poor maternal mental health in mothers of children born preterm/LBW or with HIE as compared to the general population of mothers in other low-and middle-income countries where the prevalence of maternal depression is estimated at 19-25% [47]. This finding is among the highest ranges in studies of poor maternal mental health from low-and middle-income countries (4.9-59.4%) [19].
Three-quarters of the children in our study screened positive for potential caregiver-reported disability and odds of poor mental health were more than double among mothers caring for children with a caregiverreported disability. Similar findings were noted in Malawi where 41.2% of caregivers of children with disability, including preterm/LBW and HIE children, reported having psychological distress [48]. Caring for a child with disability can increase stress in a caregiving role, increasing risk for poor mental health. Maternal depression and negative mother-infant interactions can be exacerbated when depressed mothers perceive their infants as temperamentally difficult [10]. This finding highlights the need to provide routine mental health screening and interventions to support mothers of children with developmental difficulties and disability.
In this study, poor mental health was also found to be strongly associated with single marital status. Single mothers' poor mental health prevalence was three times higher than married or cohabitating women. This  finding is similar to what was found by other studies that the presence of a partner in the family is associated with greater life satisfaction and better maternal mental health outcomes [49]. This finding may suggest the benefit of having a partner present in the family who is socially, economically and psychologically supportive of the caregiving role of the mother. Being married has been shown to lead to reduced stress in caregiving roles and thus resulting in better maternal mental health outcomes [50]. Mothers with poor mental health were more likely to experience more months of adequate household food provision, a measure of household food access. This link between stress of insufficient food and poor maternal mental health has been well demonstrated in highincome setting [51], with detriment to children's outcomes [52]. Household food insecurity in our sample was found along with a high prevalence of malnutrition and developmental delays. The burden of food insecurity is likely affecting children's outcomes both through the pathway of increased maternal stress and poor mental health, but also directly because lack of adequate nutrition impedes children's development [53]. Sufficient intake of micronutrients and dietary diversity is essential for optimizing children's brain development and preventing malnutrition including anemia [54].
Poor parenting practices were associated with higher odds of poor maternal mental health. In our sample, three fourths of children were exposed to violent discipline and nearly half were exposed to inadequate care with rates of both negative parenting practices significantly higher among mothers with poor mental health status. The overall high rates of harsh disciplinary practices for all children in our study were not surprising, as these practices have been shown to be common in Rwanda and other sub-Saharan African countries [55].  This higher rate among mothers with poor mental health is supported by other studies demonstrating the increased risk of child abuse and neglect among mothers with mental health problems [56]. Further, children with caregiver-reported disabilityof whom there were many in our samplemay experience violence more than non-disabled children from the time they are born [57]. Additionally, both poor maternal mental health and negative mother infant interactions can be exacerbated when a mother is perceiving her infant as having a disability [10]. These forms of compounded adversity are known to be detrimental to children's development. Holistic, integrated programs addressing maternal mental health, social needs for caregivers of children with developmental difficulties, and children's health, nutrition and developmental services are needed to optimize nurturing care among at-risk children. These services should be targeted to families with high-risk for poor outcomes, especially children born preterm/LBW and with HIE. Our study has a few limitations. First, the sample size was small and from only one rural Rwandan district so our findings may not be generalizable to other regions. However, Kirehe district is a rural district with similar characteristics to other rural Rwandan districts. Child disability was reported by caregivers, and no diagnostic tool was used to confirm the child's disability. However, we used a standard tool and our study was limited to biological mothers who are the primary caregivers to their child and are able to identify perceived disability of their child. In addition, as we are looking only at a cross-sectional study when children were ages 24-47 months, we have a period prevalence for poor maternal health but do not know the timing of onset or duration of poor mental health which means we cannot know what is a cause of versus a result of poor maternal mental health.

Conclusions
More than half of caregivers of children born preterm, LBW and with HIE had poor mental health status, and the children had high rates of developmental delay and a caregiver-reported disability at ages 2-3 years. Services for children with perinatal risk factors must include provision of mental health screening and treatment for mothers while simultaneously addressing early intervention and care for the child's health, nutrition, and development.