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aternal stress and depressive symptoms associated withality of developmental care in 25 Italian NICUs:cross sectional observational study

sario Montirosso a,*, Claudia Fedeli a, Alberto Del Prete b, Guido Calciolari c,nato Borgatti d NEO-ACQUA Study Group1

Centre for the Study of Social Emotional Development of the At-Risk Infant, Scientific Institute, IRCCS Eugenio Medea, Bosisio Parini,

o, Italy

partment of Neonatal Care and Neonatal Intensive Care Unit, Manzoni Hospital, Lecco, Italy

velopment Care Study Group, Italian Neonatology Society, Italy

uropsychiatry and Neurorehabilitation Unit, Scientific Institute, IRCCS Eugenio Medea, Bosisio Parini, Lecco, Italy

T I C L E I N F O

le history:

ived 16 July 2013

ived in revised form 29 October 2013

pted 3 November 2013

ords:

elopmental care

ernal stress

management

partum depression

erm infant

A B S T R A C T

Background: Parents of very preterm infants are at great risk for experiencing stress and

depression. The so called developmental care oriented approach used in Neonatal

Intensive Care Units have beneficial effects for parents. However the actual level of

developmental care may vary among units and little is known about how the routine

adoption of developmental care affects maternal stress and depression.

Objectives: To investigate the extent to which level of quality of developmental care

routinely carried out in 25 tertiary Neonatal Intensive Care Units across Italy affects

maternal stress and depression.

Participants: 178 mothers of healthy very preterm infants with gestational age �29 wk

and/or birth weight �1500 g and without documented neurologic pathologies were

recruited consecutively. 180 full-term mothers were recruited as the control group.

Methods: To distinguish the quality of developmental care level, each unit was assessed

using a specifically developed questionnaire. We compared negative emotional states of

mothers by splitting the 25 Neonatal Intensive Care Units into units with high-care and low-

care based on median splits for two main care factors: (1) The Infant Centered Care index

(consisting of measures of parent involvement, including ability to room in, frequency and

duration of kangaroo care and nursing interventions aimed at decreasing infant energy

expenditure and promoting autonomic stability). (2) The Infant Pain Management index

(consisting of measures to decrease painful experiences including pharmacologic and

nursing care practices). Maternal stress was assessed by the Parental Stressor Scale: Neonatal

Intensive Care Unit questionnaire. Maternal depressive symptomatology was assessed by

the Edinburgh Postnatal Depression Scale questionnaire.

Results: Preterm mothers from low-care units in the Infant Pain Management reported

higher scores in their perception of stress associated with behavior and appearance of the

infant than mothers from high-care units (p = 0.05). Preterm mothers from high-care units

in the Infant Pain Management reported a depressive symptomatology score average

similar to that reported by full-term mothers. No significant Infant Centered Care effect

was found both for maternal stress and depression.

Corresponding author. Tel.: +39 031 877494.

E-mail address: rosario.montirosso@bp.lnf.it (R. Montirosso).

See Appendix A for NEO-ACQUA Study Group.

Contents lists available at ScienceDirect

International Journal of Nursing Studies

journal homepage: www.elsevier.com/ijns

ease cite this article in press as: Montirosso, R., et al., Maternal stress and depressive symptoms associated with quality developmental care in 25 Italian NICUs: A cross sectional observational study. Int. J. Nurs. Stud. (2013), http://

x.doi.org/10.1016/j.ijnurstu.2013.11.001

0-7489/$ – see front matter � 2013 Elsevier Ltd. All rights reserved.

://dx.doi.org/10.1016/j.ijnurstu.2013.11.001

R. Montirosso et al. / International Journal of Nursing Studies xxx (2013) xxx–xxx2

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What is already known about the topic?

� Parents of very preterm infants are at great risk forexperiencing stress and depression.� Developmental care in NICUs has beneficial effects for

parents.� However, the actual level of developmental care may

vary among units and little is known about how theroutine adoption of developmental care affects maternalstress and depression.

What this paper adds

� The study demonstrates the relationship betweenvariations in developmental care in NICUs and maternalstress and depression.� Routine adoption of procedures designed to create a

care-oriented approach show a differential contributionto dampening the distress of mothers.� Some practices do not mitigate maternal distress, while

others promote a reduction of stress and depression inmothers of preterm infants.

1. Introduction

Parents of very preterm infants are at greater risk forexperiencing stress and depression following the infant’sbirth than mothers of full-term infants (Lefkowitz et al.,2010; Carter et al., 2005). Increased parenting distress ingeneral is an important risk factor, as it may interfere withattachment (Kaaresen et al., 2006) maternal sensitivity toinfant cues (Zelkowitz et al., 2007) and consequentlyincrease the risk for problematic long-term outcomes(Muller-Nix et al., 2004). Furthermore, parenting distressrelated to preterm birth has also been found to be animportant risk factor for long-term outcomes (Saylor et al.,2003). Consequently, reduction of parental distress is animperative target, and several studies have reportedevidence for the effectiveness of parental support duringNICU hospitalization (Brett et al., 2011) which can helpparents reduce distress levels (Shields-Poe and Pinelli,1997). Apart from standardized intervention programs(e.g., Creating Opportunities for Parent Empowerment:COPE; Mother–Infant Transaction Program: MITP), there isevidence that the so called care-oriented approach whichprovides support to mothers in NICUs and involves them ininfant’s care reduces stress and depression (Browne andTalmi, 2005; Flacking et al., 2012). The care-oriented

approach is related to the implementation of develop-mental care (DC) practices and procedures in the careprovided to premature infants and their families (Byers,2003). DC includes a broad category of interventionsdesigned to minimize the stress of the NICU environmentand to manage the care of the premature infant, such as:

control of external stimuli (vestibular, auditory, visual,tactile), kangaroo care and parental involvement (e.g.,breastfeeding, the policies of NICUs toward parentalvisiting, promoting infant–parent bonding), developmen-tal activities of daily living (i.e., nesting, swaddling, proneposition) and infant pain management (Symington andPinelli, 2006; Coughlin et al., 2009). Although the effect ofthe DC practices and procedures is still debated, rando-mized, controlled studies have documented its beneficialeffects not only for preterm infants (Slevin et al., 2000; Alset al., 2004) but also for their parents, as well (Browne andTalmi, 2005; Matricardi et al., 2013). There is evidence thatcare practices supporting physical and emotional closenessbetween the parent and preterm infant decrease theprevalence of maternal depression and distress (Melnyket al., 2006; de Alencar et al., 2009), kangaroo caresignificantly reduces maternal anxiety (Tessier et al., 1998)and depressive symptoms (Bigelow et al., 2012). Inaddition, although more research is needed (Furman,2007), providing maternal breast milk to preterm infantswas correlated with reduced maternal depression andmore maternal affectionate touch during mother–infantinteractions (Feldman and Eidelman, 2003). Parentaldistress is positively related to parental concerns aboutinfant pain (Franck et al., 2005) and infant pain is stronglydistressing for parents (Franck et al., 2012). However,parents experienced relief from distress when they wereprovided with information about infant pain, were activelyinvolved in parenting and giving comfort to their infant,received support and encouragement to be involved ininfant comfort from clinical staff (Franck et al., 2012;Axelin et al., 2010) and when they realized that staffprovided comfort to their infant (Gale et al., 2004; Francket al., 2011).

Although the beneficial effects of care-oriented practiceson parental stress and maternal symptoms of depressionhas been researched in individual NICU units, no multi-center study has investigated the question of how thecombination of different kinds of DC practices might beassociated with parental distress. Moreover, a critical pointis that the utilization of DC in practice is not yet uniformlyapplied in NICUs and recent multicenter research offersinsight about the variability between units (Ashbaughet al., 1999). For example, an inquiry in eight Europeancountries reported that parental visiting was allowed overthe 24 h period in most countries, especially in northernEurope and the UK, however in Spain and Italy just lessthan one-third of NICU allowed access at any time for bothparents (Greisen et al., 2009). A recent study (Bonet et al.,2013) has compared breastfeeding rates at discharge forvery preterm infants among eight European regions.Overall exclusive and mixed breastfeeding rates variedfrom 19% in Burgundy (France) to 70% in Lazio (Italy),suggesting that variations among units may be explained

Conclusions: The findings suggest that implementing more practices useful to reduce

infants’ painful experience can mitigate the stress and depressive symptomatology of the

preterm mothers.

� 2013 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Montirosso, R., et al., Maternal stress and depressive symptoms associated with qualityof developmental care in 25 Italian NICUs: A cross sectional observational study. Int. J. Nurs. Stud. (2013), http://dx.doi.org/10.1016/j.ijnurstu.2013.11.001

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R. Montirosso et al. / International Journal of Nursing Studies xxx (2013) xxx–xxx 3

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breastfeeding promotion practices, which have beeneloped in some hospitals independently of level ofdical care or unit size. Consequently, it is quite possiblet NICUs integrate some form of DC in their conventionale and units might have different levels of quality of DC.ferences in the actual level of quality of DC incorporated

NICU’s standard care have been evaluated in relation to infant neurobehavior (Montirosso et al., 2012a),

ever the relation between level of care routinely usedICUs and parental distress is still mainly unknown.

In the current study, we evaluated the relationsween the quality of DC typically carried out in 25ian NICUs and the negative emotional states of mothers., stress and depressive symptomatology). To evaluate

level of DC in NICUs we used a specifically developedstionnaire, the Neonatal Adequate Care for Quality of

(NEO-ACQUA) Quality of Care Questionnaire (QCQ,lu et al., 2006). We compared negative emotional states

others by splitting the 25 NICUs into units with high low quality of DC and then examining if maternalss levels were associated with levels of quality of care.

hypothesized that lower levels of quality of DC wouldelated to higher levels of maternal stress. A second aim

investigated was whether quality of DC could mitigateternal depressive symptoms. While the stress asso-ed with admission to the NICU of a preterm infant may

evaluated only in mothers of preterm infants, maternalptoms of depression can be compared with those of

-term mothers. Accordingly, we included a controlup of full-term mothers, whose depressive symptoma-gy was compared with that of preterm mothers fromUs with low and high quality of care. We expected thatpreterm mothers a high quality of care would be

ociated with lower depressive symptomatology, similarevels reported in mothers of full-term infants.

ethods

Participants

The research is part of the NEO-ACQUA project, alticenter, longitudinal study on the relationshipween the quality of care received by infants in thenatal period and their subsequent outcomes andlity of life at school age (Montirosso et al., 2012a,b).

study design includes behavioral, cognitive andotional follow-up assessments until 7 year of age of

children. An additional goal of the NEO-ACQUA study,ich is an objective of the current paper, is to evaluate toat extent the quality of care received by preterm infants

ICUs is associate with maternal emotional distress at time of the infant’s discharge.178 mothers of healthy very preterm infants wereruited consecutively by 25 tertiary care NICUs acrossy between January 2006 and December 2007. Pretermnts were recruited according to the following inclusioneria: gestational age �29 wk (range: 23–35 wk) and/orh weight �1500 g (range: 515–1928 g), no documentedrologic pathologies as shown by cerebral ultrasoundriventricular leukomalacia up to stage 1; intraventri-ar hemorrhage up to stage 1 or 2), no sensory deficits

(retinopathy up to stage 1 or 2), neonatal hearing screening(ABR or otoemissions) within the norm at the 34th week,and no malformation syndromes and/or major malforma-tions. Eligible mothers were contacted during the hospi-talization of their preterm infants and the data werecollected in the pre-discharge week. A group of 180mothers of full-term infants (gestational age �37 wk andbirth weight >2500 g) were selected from the sequentialregister of births held in the delivery ward of theparticipating hospitals by sampling every birth notadmitted to the NICU. Full-term infants were healthy,with no pathologies and risk factors in pregnancy andduring the perinatal period. Mothers were eligible if theymatched on maternal age (�5 years), maternal educationlevel, family socioeconomic status and marital status.Mothers were selected at random to be recruited as a controlgroup and approached several days after the infant’s delivery.Data were collected within 3–5 days after the infant’s birth.For mothers of both groups the inclusion criteria were thefollowing: Italian nationality, age over 18 years, no manifestpsychiatric and cognitive pathologies, no drug addiction, nosingle-parent families. The study was approved by the EthicsCommittees of the participating hospitals. All mothersinvolved in the NEO-ACQUA study signed a written informedconsent form.

3. Measures

Perinatal data collection. Perinatal variables collectedincluding gender, gestational age, birth weight, multiplebirth, Apgar scores, intrauterine growth status classified asappropriate for gestational age or small for gestational age.

Socio-demographic questionnaire. Socio-demographicdata such as parental age, years of study and occupationalstatus were obtained for both parents using a question-naire. According to Hollingshead’s classification (1975),the more prestigious occupational level between motherand father was considered to be the family socio-economicstatus (SES). Score ranges from 0 (occupations that do notrequire high school graduation) to 90 (occupations thatrequire highly specialized education and training). Lowerscores reflected lower socio-economic status.

Maternal stress. Maternal stress was assessed by theParental Stressor Scale: Neonatal Intensive Care Unit(PSS:NICU – Miles et al., 1993), a 26-item self-reportmeasure of stress assessing three dimensions of parentalexperience during the NICU stay: Sights and Sounds (SS; 6items) – (stress related to the NICU physical environment)Infant Behavior/Appearance (IBA; 13 items) – (stressbecause of the infants’ appearance and behavior); ParentalRole Alteration (PRA; 7 items) – (stress related to thealteration in the expected parental role and the postpone-ment of actual parental care). Mothers were asked to rateeach item on a five-point Likert scale from ‘not stressful’ to‘extremely stressful’. Two main scores can be computed foreach subscale of PSS:NICU. Stress Occurrence Level (1) isthe level of stress produced when a situation occurs andthe stress score is computed using only those items thatmothers indicate as a source of stress. Overall Stress Level(2) computes the stress score using all the items, giving arating of 1 (not stressful) for those items not experienced

ease cite this article in press as: Montirosso, R., et al., Maternal stress and depressive symptoms associated with quality developmental care in 25 Italian NICUs: A cross sectional observational study. Int. J. Nurs. Stud. (2013), http://

x.doi.org/10.1016/j.ijnurstu.2013.11.001

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by the parent. Stress Occurrence Level (1) should be usedwhen the focus is the parent, while the Overall Stress Level(2) when the focus is the NICU environment (Miles et al.,1993). Given that the main aim of the current study is toevaluate whether the typical environmental interventionscarried out in NICUs (i.e., practices and proceduresdesigned to minimize the stress of the NICU environmentand to manage the care of the premature infant) mighteffectively alleviate stress and depression in mothers ofpreterm infants, in the current study we computed OverallStress Level (2). The Overall Stress Level is calculated foreach subscale by dividing the sum of scores for eachsubscale by the number of items making up a subscale.Each subscale ranges from 0 to 5, with lower scoresreflecting minor perceived maternal stress. The PSS:NICUhas demonstrated excellent validity and reliability instudies in North America (Miles et al., 1993), England(Franck et al., 2005) and Italy (Montirosso et al., 2012b).

Maternal depression. Depressive symptomatology wasassessed by the Edinburgh Postnatal Depression Scale(EPDS – Cox et al., 1987), which is one of the most widelyused screening tools for postnatal depression. The Italianversion of EPDS has showed psychometric propertiescomparable to those of the original version (Benvenutiet al., 1999). The EPDS is a 10-item self-report ques-tionnaire designed to measure emotional and cognitivesymptoms of depression. Each item is rated on a 4-pointscale (0–3). The sum score of items ranges from 0 to 30.According to previous studies using the EPDS for researchpurposes (Benvenuti et al., 1999) a total score 9 or higherwas taken as a cut-off for the presence of depressivesymptoms in the clinical range. Large community surveyshave shown the EPDS to have strong validity and reliability(Eberhard-Gran et al., 2001). The EPDS has been used in anumber of other studies investigating postpartum depres-sion in preterm mothers (Vigod et al., 2010) and to screenfull-term mothers at risk for postnatal depression in thefirst days postpartum (Teissedre and Chabrol, 2004).

Measure of Developmental Care. Given that there is nogenerally accepted definition of DC (Aita and Snider, 2003)we developed the QCQ (Bellu et al., 2006) to evaluate thelevel of DC in NICUs. The areas and factor analyses applied toQCQ responses are described in detail elsewhere (Montir-osso et al., 2012a,b). Two indices of DC were used: (1) TheInfant Centered Care (ICC) index, assessing parent’s involve-ment in care such as the possibility for parents to spend thenight in the unit; use of parental kangaroo care as a routineprocedure; the duration per day of kangaroo care (< or�45 min), and the presence of nursing interventions tosupport infant development by decreasing infant energyexpenditure and promoting stability, such as infant contain-ment, postural maneuvers and reduction of disturbingtactile stimulation. (2) The Infant Pain Management (IPM)index, measuring number of pharmacologic and non-pharmacologic procedures used for reducing pain duringinvasive medical procedures (e.g., intravenous lines, drai-nage tubes and endotracheal tubes), use of pharmacologicanalgesia or sedation during continuous mechanical venti-lation, the kind of blood collection procedure (i.e., heel stick)and the use of a clinical evaluation scale of newborn painand/or a protocol written for the management of newborn

pain. Based on factor weightings, a composite score for ICCand IPM indices was computed for each NICU. The ICC indexranged from 0 to 8, with higher scores indicating higher levelof ICC. The IPM index ranged from 0 to 10, with higher scoresindicating higher levels of IPM. To distinguish the quality ofcare level, each NICU was assessed as being a low-care groupor high-care group based on median splits for the ICC andIPM. This approach had the advantage of avoiding possiblebias from extreme scores. For the ICC (median = 7.50,mean = 6.56, SD = 2.42): 12 NICUs had low-quality care(97 infants) and 13 NICUs had high-quality care (81 infants).For the IPM (median = 6.00, mean = 5.48, SD = 2.53): 14NICUs had low-quality care (91 infants) and 11 NICUs hadhigh-quality of care (87 infants).

4. Statistical analysis

Preliminarily statistical analyses evaluated generalcharacteristics of the units (number of beds, totaladmission per year), perinatal data and socio-demographicvariables. Categorical variables were analyzed by chi-square tests. Continuous variables were evaluated withseparate analyses of variance (ANOVAs) by using a 2 (ICC:low and high level of care) � 2 (IPM: low and high level ofcare). To determine if the care quality level was related tomaternal stress levels a multivariate analyses of variance(MANOVA) was applied to the 3 PSS:NICU scales (SS, IBA,PRA) with a 2ICC � 2 IPM factorial design. To examinewhether differences existed in EPDS scores as function ofcare quality level and, also than the maternal depression ofthe full-term mothers, two univariate ANOVAs wereapplied, separately for ICC and IPM. Where appropriate,follow-up t-tests for group comparisons were conducted toinvestigate significant effects. For the determination ofeffect size, partial h2 for significant effects were estimated.The conventional cut-offs for partial Eta square ðh2

pÞ are0.01, 0.06 and 0.14 for small, medium and large effect sizeswere used. All analyses were performed at a significancelevel of p � 0.05, using SPSS Statistics (SPSS version 17.0 forWindows, SPSS Inc., Chicago, IL, USA).

5. Results

Infants, maternal factors and unit characteristics. Descrip-tive statistics are presented for each variable in Table 1. Nodifferences were found in general characteristics of theunits, as well as perinatal and socio-demographic data.There were no significant differences in age, marital status,or education between mothers from low and high-careNICUs or between preterm mothers and full-term mothers.

Maternal stress. The MANOVA showed no significant ICCeffects for the SS, IBA and PRA PSS:NICU scales. Asignificant IPM effect emerged for stress related to IBA,F(1, 101) = 5.53, p = 0.05, h2

p ¼ 0:05. Mothers from low IPMNICUs reported higher scores in their perception of stressassociated with behavior and appearance of the infant thanmothers from high-care units (M = 3.49, DS = 0.92 vs.M = 3.01, DS = 0.91) in infant pain control (see Fig. 1).

Maternal depression. Overall, the percentage of motherswith EPDS scores > 9 was 54.3% (N = 95) in preterm groupand 31.1% (N = 56) in the full-term group (x2 = 19.50,

Please cite this article in press as: Montirosso, R., et al., Maternal stress and depressive symptoms associated with qualityof developmental care in 25 Italian NICUs: A cross sectional observational study. Int. J. Nurs. Stud. (2013), http://dx.doi.org/10.1016/j.ijnurstu.2013.11.001

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R. Montirosso et al. / International Journal of Nursing Studies xxx (2013) xxx–xxx 5

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0.000). As for NICUs quality of care, the percentage ofterm mothers from low ICC NICUs with EPDS scores > 9s 54.6% (N = 53 of 97), while mothers from high ICCUs was 53.8% (N = 42 of 78; x2 = 0.00, p = 0.966). Thecentage of preterm mothers from low IPM NICUs withS scores > 9 was 76.1% (N = 67 of 88), while mothers

high IPM NICUs was 32.2% (N = 28 of 87; x2 = 33.41,0.000). Overall, preterm mothers had significantlyher EPDS scores than the control mothers (M = 10.00,

DS = 6.05 vs. M = 6.34, DS = 3.95, t(292) = �6.70, p = 0.000).As for NICUs quality of care, the ANOVA showed asignificant ICC effect, F(2, 351) = 24.45, p < 0.001,h2

p ¼ 0:12. Pairwise comparisons showed that full-termmothers reported lesser level of depression (M = 6.34,DS = 3.95) than both of preterm mothers from low-careunits (M = 10.45, DS = 6.34, t(135) = 5.78, p = 0.000) andpreterm mothers from high-care units (M = 9.63, DS = 5.68,t(110) = 4.65, p = 0.000). No difference was found in the

le 1

mary of general characteristics of the NICUs, perinatal and socio-demographic variables for the preterm mothers from high and low quality of care for

nt Centered Care index and for Infant Pain Management index and for full-term mothers.

Preterm group Full-term group

Infant Centered Care index Infant Pain Management index

Low (NICU = 12)

(N = 97, 48 F)

High (NICU = 13)

(N = 81, 43 F)

Low (NICU = 14)

(N = 91, 45 F)

High (NICU = 11)

(N = 87, 46 F)

(N = 185, 92 F)

Mean SD Mean SD Mean SD Mean SD Mean SD

tal admissions per years (N) 406.58 224.45 675.46 475.50 471.36 226.00 641.91 536.22 – –

mber of beds 19.08 9.27 22.92 12.96 20.79 10.06 21.46 13.17 – –

nght of hospitalization (days) 59.88 20.38 61.32 24.76 60.69 23.01 60.37 21.92 – –

rth weight (g) 1161.56 229.36 1091.75 258.16 1129.08 249.15 1130.54 241.36 3290.68 402.82

stational age at birth (weeks) 29.12 1.96 28.81 2.41 28.97 2.02 29.00 2.35 39.30 8.70

other’s age (years) 33.31 5.02 33.92 4.61 33.27 4.95 33.92 4.72 33.63 4.37

ucation mother (years) 12.42 3.90 12.97 3.73 12.36 4.14 12.98 3.47 12.96 3.74

S score 50.83 23.47 53.33 18.44 49.89 23.26 54.19 18.88 55.56 19.78

N % N % N % N %

rth weight �1000 g 27 27.8 33 40.7 31 34.1 29 33.3 – –

stational age �29 wk 55 56.7 48 59.3 54 59.3 49 56.3 – –

ultiple birth 0 0.0 3 3.7 1 1.1 2 2.3 – –

all for gestational age 18 18.6 21 25.9 18 19.8 21 24.1 – –

tenatal corticosteroids 72 75.0 68 86.1 65 73.0 75 87.2 – –

tent ductus arteriosus 28 28.9 24 30.0 28 31.1 24 27.6 – –

nventional ventilation 64 66.0 40 50.0 58 64.4 46 52.9 – –

gh-frequency ventilation 10 10.3 8 10.0 9 10.0 9 10.3 – –

ygen dependency at 36 wk 5 6.0 11 16.9 6 7.8 10 13.9 – –

oven or suspected

necrotizing enterocolitis

1 1.0 0 0.0 1 1.1 0 0.0 – –

H (grade 1 or 2) 14 14.4 13 16.0 17 18.7 10 11.5 – –

psis 8 8.2 2 2.5 10 11.0 0 0.0 – –

male; SES: socio-economic status, IVH: intraventricular hemorrhage.

1. Means of the scores for PSS:NICU in the preterm mothers from high and low quality of care for Infant Centered Care index and for Infant Pain

agement index.

.05. SS: Sights and Sounds; IBA: Infant Behavior/Appearance; PRA: Parental Role Alteration.

ease cite this article in press as: Montirosso, R., et al., Maternal stress and depressive symptoms associated with quality developmental care in 25 Italian NICUs: A cross sectional observational study. Int. J. Nurs. Stud. (2013), http://

x.doi.org/10.1016/j.ijnurstu.2013.11.001

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preterm group between mothers from low and high ICCNICUs. A significant effect was found for IPM, F(2,351) = 54.76, p < 0.001, h2

p ¼ 0:24). Pairwise comparisonsshowed that preterm mothers from low-care unitsreported higher level of depression (M = 12.74, DS = 5.97)both related to full-term mothers (M = 6.34, DS = 3.95,t(123) = 9.08, p = 0.000) and to preterm mothers from high-care units (M = 7.42, DS = 4.87, t(172) = 6.43, p = 0.000).No difference was found between preterm mothers fromhigh-care units and full-term mothers (see Fig. 2). In allanalyses the effect sizes were in general small to large(range: 0.05–0.24).

6. Discussion

The main objective of the current study was toinvestigate whether the level of quality of DC found in alarge number of NICUs was associated with maternal stressand depressive symptomatology. Unexpectedly, for the ICCindex there were no differences in stress levels betweenmothers from high and low quality-of-care NICUs.Furthermore, consistent with previous studies, pretermmothers reported higher symptoms of depression thanfull-term mothers (Davis et al., 2003), but a high quality ofcare for ICC did not mitigate maternal depressive

symptomatology. The result is not readily explained,however a possible interpretation of this lack of differenceis that ICC aggregated several aspects of care practicesroutinely used in NICUs, making it less sensitive to thedifferences in the extent of maternal distress levels. On theother hand, the finding that only implementing DCpractices routinely used in NICUs might not be particularlyeffective in alleviating maternal stress should not be sosurprising. A body of evidence suggests that in the NICUs,the maternal negative emotional states are mitigatedwhen direct mother–infant interactions are supported;that is, when the mother is involved in nutritive activities,such as holding, touching and communicating with theirinfant (Welch et al., 2012). Overall, these kind ofinterventions are addressed to increase parental abilityto recognize signs of stress and well-being, help them tosoothe their infant and to use appropriate stimulation andto improve the physical contact between parents and theirinfant to encourage parent-infant proximity (Boukydis,2008; Newnham et al., 2009). Interestingly, parents whoparticipated in focused interventions reported lower stresslevels of anxiety and depression than parents who receivedstandard support (Matricardi et al., 2013; Melnyk et al.,2006). Accordingly, our results indicate some DC practices,such as the possibility for parents to spend the night in the

Fig. 2. Means of the scores for EPDS in the preterm mothers from high and low quality of care NICUs mothers, subdivided for Infant Centered Care index and

for Infant Pain Management index, and for full-term mothers.

***�0.001

Please cite this article in press as: Montirosso, R., et al., Maternal stress and depressive symptoms associated with qualityof developmental care in 25 Italian NICUs: A cross sectional observational study. Int. J. Nurs. Stud. (2013), http://dx.doi.org/10.1016/j.ijnurstu.2013.11.001

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t or the possibility to practice parental kangaroo care do guarantee per se a reduction of maternal negativeotional states, providing indirect evidence that moreused interventions might be needed to address parentalress (Boukydis, 2012).

Our findings suggested that the control of infant pain a specific relation to maternal stress and depressiveptomatology. Mothers from high quality of care

Us for the IPM reported lower levels of stress relatedbehavior and appearance of the infant and lowerternal depressive symptomatology, suggesting thatnt pain management care interventions were criticaloderating maternal stress related to the sight of one’s

nt. In a previous study, preterm infants from lowlity of care NICUs, for the IPM factor had lower levelsttention and arousal, were more lethargic, and had

re non-optimal reflexes. This suggests that lower paintrol practices in NICUs may contribute to reducing thent’s neurobehavioral stability (Montirosso et al.,2a). Moreover, control of pain likely reduces physio-

ic and behavioral changes, energy expenditure, andtability (Grunau, 2003). Thus, the control of pain iscial to positively influencing infant behavior andearance (e.g., facial expressions) which in turn coulduce maternal distress. Evidence suggests that some of

greatest sources of stress for parents include infantearance and that parental distress is positively relatedh concerns about infant pain. In addition, the mostent source of stress is witnessing painful proceduresicted on one’s infant (Franck et al., 2005). Parentsorted that their inability to reduce the infant’s pain,ng with unmet information needs about their infant’sn are potent stressors (Axelin et al., 2010; Gale et al.,4). Therefore, even a routine use of care practices (asosed to ad hoc interventions) directed at minimizingnt’s pain may help to alleviate maternal stress andressive symptomatology. It is quite possible that inUs with high IPM, maternal distress could have beendiated by parents’ perception that some interventions., non-pharmacologic treatments, such as non-nutri-

sucking, swaddling) provide by staff were effective innaging their infant’s pain. Previous studies suggestedt during the NICU stay, parents experience relief fromtress when they realized that staff provided comfort toir infant (Gale et al., 2004; Franck et al., 2011). A recentlticenter study has corroborated the presence of largeerences between NIUCs in pain control proceduresvided by the staff to premature infants; particularly,non-pharmacological procedures which are easily

ervable by parents (Losacco et al., 2011). Thus, it is notprising that mothers from different units could haven relevant differences in the staff approach to infantn. Whatever is the ultimate explanation, it iseworthy that preterm mothers from high quality ofe NICUs for infant pain control reported depressive

ptomatology score means similar to that reported inthers of full-term infants. Thus, our findings confirmt it is important to improve the control of neonataln during hospitalization, not only for preventingerse consequences for the infants (Axelin et al.,0), but also because it has a buffering role protecting

against stress and depressive symptomatology of pre-term mothers.

The study has limitations. First, although a substantialstrength of the current study is the use of data from a highnumber of NICUs that were geographically diverse, the 25NICUs sampled self-selected themselves into the NEO-ACQUA study and cannot be considered representative ofDC quality in all 120 Italian NICUs. Second, the indexeswere derived from factor analyses of the informationgathered on the DC, but not all aspects of DC wereexamined, and other aspects of care may have influencedmaternal distress (i.e., breastfeeding). Third, because theindexes aggregated several aspects of care practices, it isnot possible to establish which particular aspects affectedthe presence of maternal distress.

In spite of these limitations, the study provides someimplications for DC practices in NICUs. Our findingsindicate that mothers of healthy very preterm infantscontinue to experience significant levels of stress/depres-sion despite more open access to intensive care units andmore use of some DC practices routinely proposed byNICUs. Thus, while some DC activities might be notsufficient to alleviate maternal stress, our results indirectlysupport the view that more comprehensive interventionsfocused on caregiving, nurturing and relational activitiesmight be more appropriate both to improve neurodeve-lopmental outcomes of premature infants (Milgrom et al.,2010) and to alleviate mothers’ emotional negative states(Matricardi et al., 2013). The findings reported here alsosuggest that implementing more practices useful to reduceinfants painful experience into a NICU’s conventional carecan mitigate stress and depressive symptomatology of thepreterm mothers experienced during the NICU stay. Inparticular, the inclusion of the control group in this study isan important strength which allowed for the comparisonof NICU mothers’ depression related to quality of care withthe depressive experience of mothers of non-NICU infants.In clinical practice, minimizing painful procedures whenfeasible becomes critical, not only for infants’ neurobeha-vioral maturation (Montirosso et al., 2012a), but also forthe mothers of preterm infants who could experience adepression level comparable to that of mothers of full-terminfants.

In conclusion, our results extend the research in thisarea by showing that routine adoption of proceduresdesigned to create a care-oriented approach showed adifferential contribution to lowering the distress ofmothers having an infant admitted to the NICU. SomeDC practices do not mitigate maternal distress, whileothers promote a reduction of stress and depression inmothers of preterm infants. The evidence in this studyseems to suggest that a generic assumption that some DCprocedures embedded in clinical practice are intrinsicallyhelpful for parents would, at the best, be limited. Instead,NICU staff need to consider that the participation ofparents in the care of their preterm requires efforts toreduce maternal distress by specific interventions. Moreresearch is needed in this area to guide our understandingof which specific kinds of DC typically carried out in NICUsmight effectively alleviate stress and depression inmothers of preterm infants.

ease cite this article in press as: Montirosso, R., et al., Maternal stress and depressive symptoms associated with quality developmental care in 25 Italian NICUs: A cross sectional observational study. Int. J. Nurs. Stud. (2013), http://

x.doi.org/10.1016/j.ijnurstu.2013.11.001

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Acknowledgements

The members of the NEO-ACQUA Study Advisory Boardare: Roberto Bellu, Renato Borgatti, Maria Caterina Cavallo,Alberto Del Prete, Guido Calciolari, Rosario Montirosso,Rinaldo Zanini. Thanks go to the MediDataStudi e Ricerchestaff in Modena for their organizational, technical,scientific support. We are very grateful to the staff of allthe 25 participating units. We are deeply indebted to ZackBoukydis for his useful comments and suggestions on allaspects of the text of the earlier draft. Finally, we wouldlike to thank the parents who participated in the study.

Conflict of interest: There are no financial disclosures orconflicts of interest for any authors.

Funding: The NEO-ACQUA project was supported by anunrestricted educational grant from Chiesi FarmaceuticiS.p.A.

Ethical approval: The study was approved by the EthicsCommittees of the 25 participating hospitals.

Appendix A

NEO-ACQUA Study Group: Fabio Mosca, Odoardo Picciolini,

NICU, Department of Maternal and Pediatric Sciences, Uni-

versity of Milan Fondazione IRCCS Ca’ Granda, Milan, Italy.Stefano Visentin, Nadia Battajon, Neonatology and NICU, Ca’

Foncello Hospital, Treviso, Italy.Maria Lucia Di Nunzio, Fiorina Ramacciato, NICU, Cardarelli

Hospital, Campobasso, Italy.Laura Barberis, Emmanuele Mastretta, Division of Neonatology

and NICU, S. Anna Hospital, Turin, Italy.Rinaldo Zanini, Roberto Bellu, NICU, Manzoni Hospital, Lecco,

Italy.Giovanna Carli, Michela Alfiero Bordigato, NICU, Hospital of

Camposampiero, Camposampiero Italy.

Valeria Chiandotto, Cristiana Boiti, Department of Neonatol-

ogy, University Hospital S. M. M., Udine, Italy.Rosangela Litta, Giovanna Minelli, Division of Neonatology and

NICU, Ospedali Riuniti, Foggia, Italy.Marcello Napolitano, NICU, Evangelic Hospital Villa Betania,

Napoli, Italy.Alessandro Arco, NICU, University Hospital G. Martino, Mes-

sina, Italy.Palma Mammoliti, NICU, Ospedale degli Infermi, Rimini, Italy.Cinzia Fortini, NICU, PediatricUniversity Hospital, Ferrara,

Italy.Paolo Tagliabue, Neonatology, San Gerardo Hospital, Monza,

Italy.Lorenzo Quartulli, NICU, Perrino Hospital, Brindisi, Italy.Giuliana Motta, NICU, Niguarda Hospital Ca’ Granda, Milan,

Italy.Paola Introvini, NICU, Buzzi Hospital, Milan, Italy.

Rosetta Grigorio, NICU, Umberto I Hospital, Siracusa, Italy.

Paola Mussini, NICU, C. Poma Hospital, Mantova, Italy.

Giulia Pomero, NICU, Santa Croce e Carle Hospital, Cuneo, Italy.Carlo Poggiani, NICU, Istituti Ospitalieri, Cremona, Italy.

Ananda Bauchiero, Department of Neonatology, S. Anna Uni-

versity Hospital, Turin, Italy.

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