PEDIATRICS Vol. 121 No. 5 May 2008, pp. e1267-e1278 (doi:10.1542/peds.2006-2510)
ARTICLE |
Lower Stress Responses After Newborn Individualized Developmental Care and Assessment Program Care During Eye Screening Examinations for Retinopathy of Prematurity: A Randomized Study
a Department of Women and Child Health, Karolinska Institute, Stockholm, Sweden
b Departments of Paediatrics
f Ophtalmology, Lund University, Lund, Sweden
c Winnicott Baby Unit, St Mary's National Health Service Trust, London, United Kingdom
d Department of Paediatrics, Linköping University, Linköping, Sweden
e Northwick Park Hospital, London, United Kingdom
g Department of Optometry and Visual Science, City University, London, United Kingdom
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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OBJECTIVE. Screening examination for retinopathy of prematurity is distressing and painful. The aim of the present study was to investigate whether a Newborn Individualized Developmental Care and Assessment Program intervention during a retinopathy of prematurity examination results in less adverse behavioral, pain, and stress responses as compared with standard care.
METHODS. The first 2 eye examinations in 36 preterm infants were evaluated. The infants were randomly assigned at the first eye examination to receive either Newborn Individualized Developmental Care and Assessment Program care or standard care. At the second examination, crossover of subject assignment was performed. The assessments included behavioral responses; recordings of heart rate, respiration, and oxygenation; pain scores (premature infant pain profile); and salivary cortisol at defined time points up to 4 hours after the eye examination. The nursing support given during the eye examinations (intervention score) were scored using predefined criteria.
RESULTS. Altogether, 68 examinations were evaluated. Newborn Individualized Developmental Care and Assessment Program care was associated with better behavioral scores during the examination but there was no difference in heart rate, respiratory rate, oxygenation, or premature infant pain profile score between the 2 care strategies before or after the eye examination. Salivary cortisol increased from baseline to 30 minutes after the eye examination independent of care strategy and decreased significantly between 30 and 60 minutes when infants were subjected to Newborn Individualized Developmental Care and Assessment Program care but not after standard care. During the study period the intervention score for standard care increased and approached the score for Newborn Individualized Developmental Care and Assessment Program care at the later eye examinations.
CONCLUSION. A Newborn Individualized Developmental Care and Assessment Program-based intervention during eye examination does not decrease pain responses but results in faster recovery, as measured by lower salivary cortisol 60 minutes after the examination. The differences were seen despite the influence from the Newborn Individualized Developmental Care and Assessment Program intervention on the standard care treatment that occurred during the study period.
Key Words: developmental care • eye examination • NIDCAP • pain • preterm infant • retinopathy of prematurity • stress
Abbreviations: ROP—retinopathy of prematurity • NIDCAP—Newborn Individualized Developmental Care and Assessment Program • PMA—postmenstrual age • PIPP—premature infant pain profile
The screening examination for retinopathy of prematurity (ROP) can be stressful for the preterm infant. Several studies have reported transient increases in blood pressure, heart rates, and respiratory rates, as well as decreased oxygen saturation.1–5 Behavioral responses and crying have been observed at several time points during the procedure, including before the examination when eye drops were administered, during the examination when an eyelid speculum was inserted, and during manipulation of the eye.4,5 The mydriatic eye drops given before the eye examination have also been associated with other adverse effects such as apnea, acute gastric distention, feeding difficulties, and necrotizing enterocolitis.6–8
Several strategies for preventing procedural pain and distress in preterm infants are known and include skin-to-skin contact, environmental and behavioral strategies, and oral sucrose.9–14 Slevin et al,15 showed that preterm infants, who were "nested," that is, bedded in a nest-like manner with soft boundaries, during ROP examinations displayed significantly less discomfort, as judged by movement activity and crying. However, intervention with "comfort care" with infants swaddled, held, and given 24% sucrose solution from 15 minutes before to 15 minutes after the eye examination did not affect "vital signs" (ie, pulse rate, respiratory rate, and oxygen saturation) as compared with a control group.16
Newborn Individualized Developmental Care and Assessment Program (NIDCAP)17 is an intervention program aiming at optimizing and adapting neonatal care for preterm infants. Individual intervention recommendations are created from structured observations of the infant's behavioral responses during a care procedure.18 Influences from NIDCAP have changed the overall care of preterm infants in many NICUs. An increasing number of NICUs have adopted developmental care strategies, for example, undisturbed periods, incubator covers, bed support, and reduction in environmental light and noise, without the individualized component of NIDCAP. It has been shown previously that short NIDCAP-based interventions ("developmental care" interventions) may exert positive influences on pain and stress responses during routine care procedures, for example, diaper changes or weighing.11,12 The hypothesis of the present study was that a short NIDCAP-based intervention during eye examination for ROP results in less distress and pain. More specifically, the aim of the present study was to investigate whether NIDCAP care during ROP examinations results in less adverse behavioral responses, lower pain scores, and lower stress responses during and after an eye examination, as compared with standard care.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Thirty-six preterm infants (gestational age <32 weeks) in 2 tertiary level NICUs, St Mary's Hospital, (London, United Kingdom) and the University Hospital of Lund (Lund, Sweden), were included in the study. The study design used randomization with 2 time points and crossover of subject assignment to the treatment and control groups. This was done repeatedly in some infants (
6 examinations). In the present evaluation, the results of the first 2 eye examinations are presented, 1 with NIDCAP care and 1 with standard care in a randomized order. The study has the characteristics of a pilot study, and no formal power estimation was performed before the study. The aim was to include 20 infants at each center, altogether 40 infants, which, in several studies evaluating care interventions in preterm infants, have been sufficient to show significant differences.11,12 During the study period, the routines for eye examinations changed in London, and, therefore, only 16 infants were included at this center. Before the study, clinical routines were compared between the 2 units, and clinical data were prospectively collected accordingly. The study was approved by the research ethics committees at St Mary's Hospital and Lund University Hospital, and informed parental consent was obtained before the study. The study started 1 hour before the eye examination and ended 4 hours after the examination. The random assignment was performed before the first eye examination by using sealed envelopes in blocks of 4 (2 NIDCAP care and 2 standard care). Evaluations of responses to the eye examinations were made by recordings of behavioral responses, heart rate, respiration and oxygenation, oxygen administration, pain scores, and salivary cortisol. An overview of the study is given in Table 1. Administration of oral sucrose or glucose was not part of standard treatment for ROP examinations in either unit. Additional oxygen was administered by the neonatal staff according to local guidelines; recommended oxygen saturation levels were 87% to 92% in London and 88% to 92% in Lund.
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The 2 NICUs in London and Lund have NIDCAP-certified staff and partly implemented NIDCAP. A majority of the neonatal staff in London had attended informal NIDCAP education, and a majority of the neonatal staff in Lund had attended introductory NIDCAP lectures, including bedside training. The NICU in Lund is 1 of 2 units constituting the Scandinavian NIDCAP Center (the other unit being the NICU at Karolinska Hospital, Stockholm, Sweden). The 2 units in London and Lund differ in several aspects, including strategies for surfactant administration and blood transfusions. The ethnicities of the 2 populations also differ with more African and Indo-Pakistani infants in London. The NICU at St Mary's Hospital has 18 beds with 2 to 7 infants in each room, and the NICU in Lund has 22 beds with 2 to 3 infants in each room. The methods for eye examinations differ between the 2 hospitals, as described below.
In London, the eye examinations were performed by digital imaging (RetCam 130, Pleasanton, CA) screening. A contact lens coupling fluid (Viscotears, Novartis, Frimely, Camberley, Surrey, United Kingdom) was applied onto the cornea and the camera lens placed on it. Eyelids were held open by a speculum, and a scleral indenter was used only occasionally. Pupillary dilatation was obtained with cyclopentolat 0.5% and phenylephrine 2.5% instilled 60 minutes before examination. Some infants, mainly brown eyed, needed a second dose of eye drops to obtain adequate pupillary dilatation. Just before the eye examination, local-anesthetic eye drops were administered with proxymetacaine 0.5% or novesceine 0.4%, The ROP examinations were usually performed early in the morning, between 7:30 and 8:30 AM, with infants kept in incubators or in their beds. Blood samples, as clinically indicated, were taken in all of the London infants after 
1 hour of rest after the eye examination according to clinical routines.
In Lund, eye examinations were performed by indirect ophthalmoscopy with a 25-Diopters lens using indentation and lid speculum. The infants’ pupils were dilated with 0.25% cyclopentolat, 0.25% tropicamide, and 1.25% neosynephrine 1 hour before the examination. Local anesthetics in the form of 0.4% oxybuprocain were instilled before the eye examination. ROP examinations were usually performed in the morning between 9:00 and 10:00 AM. After the eye examination, the infants were usually not disturbed until the next meal 
2 hours later.
Patient data are given in Table 2. There were no differences in gestational age at birth between the 2 centers. However, at the first eye examination, the infants in London were slightly more mature, at a median 33 weeks’ postmenstrual age (PMA), as compared with the infants in Lund (median: 32 weeks’ PMA; P = .026). There were also differences in hemoglobin levels, both between London and Lund and between the 2 eye examinations (Table 2). The 2 units have different blood transfusion policies, and the lower hemoglobin in London was expected. These data were collected because an anemic infant may respond differently than an infant with higher hemoglobin values. A blood sample was taken within 1 week before the eye examination, and if several blood samples were taken, the 1 closest to the eye examination was used for this evaluation.
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Standard Care During Eye Examinations
Elements of NIDCAP care were applied to all of the infants, at both sites, and consisted of dimmed lighting, reduced sound and activity levels, and standard bed support. One caregiver assisted the ophthalmologist in Lund. In London, a caregiver was present only occasionally because of busy morning routines and hand over to the dayshift. Parents were allowed to participate during the examination, but they were not specifically encouraged in London or in Lund.
During the ROP examinations, infants were lying supine, and their heads and arms were supported by the caregiver. The nurses who supported the infants were experienced but not NIDCAP certified. They were informed about the aim of the study and were encouraged to provide "best standard care" for the infant.
NIDCAP Care During Eye Examinations
A structured, but shortened, NIDCAP observation was done before the eye examination. In London this was done the day before and in Lund before and in conjunction with the administration of eye drops 1 hour before the eye examination.
The NIDCAP care during the eye examination was performed by a NIDCAP-certified observer and aimed at performing the ROP examination with a minimum of distress for the infant. General instructions, with individual evaluation of the infant's responses, included direct support to the infant, pacing of the eye examination, and modification of the environment (Table 3). The intervention started 1 hour before the eye examination, when the first eye drops were administered. A recommendation to caregivers was explicitly given to assure the infant undisturbed rest between the eye drops and the eye examination. The neonatal staff had full access to the rooms where the ROP examinations were performed and could be asked to assist in the examinations when required. Thus, the staff was not blinded to the purpose of the study or to the intervention. Feeding times were adjusted to ensure that the infants were not stressed by hunger before the eye examinations. If the meals were given closer to the eye examination than 1 hour, gavage feeding was given slowly to prevent additional exhaustion. Because the eye examinations were performed early in the morning in London, parents were only present occasionally to comfort their infant during or immediately after the eye examination. In Lund, parents were informed of how to best support their infant, such as holding their infant's hands softly and talking with a soothing voice. All of the eye examinations were performed in the infant's bed or incubator.
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Evaluation of Responses to the Eye Examinations
The different time points for the evaluations are given in Table 1.
Behavioral Evaluation
The clinical behavioral responses were assessed by observing the infant during a 2-minute period according to the Synactive model19 and by scoring the following: color (3 = healthy color, pink or red/pale; 2 = pink or red/pale with some duskiness, webbed, or paleness; and 1 = poor color, without any sign of healthy color); breathing (3 = stable, regular 40–60 breaths per minute; 2 = intermediate, irregular, some regularity, fast, deep or shallow, or short pauses; and 1 = unstable, irregular with pauses, or any other combination without regularity in it); muscle tone (3 = modulated, 2 = some modulation, some low tone such as gape face, or some hyperextension, and 1 = completely flaccid or completely hypertone); state and state regulation (3 = deep sleep, light sleep, or calm alertness; 2 = drowsy, not asleep or awake; and 1 = motor aroused or crying); position (side, prone, or supine); heart rate; breathing rate; and oxygen saturation. In London, the assessments were performed by 3 NIDCAP-certified individuals (Inga Warren, Zoe Khan and Jane Buffery, St Mary's Hospital, London, United Kingdom) trained by Dr Kleberg, the first author of this article. In Lund, all of the evaluations were made by an experienced neonatal nurse, who is not NIDCAP certified (Ms Berg). To evaluate interobserver agreement, Ms Berg and Dr Kleberg, who is an NIDCAP trainer, performed 30 test observations, and reached an interrater agreement of 0.74 (Cohen's 
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Evaluation of Heart Rates, Respiratory Rates, and Oxygenation
An assessed average and ranges of heart rates, respiratory rates, and oxygen saturation levels were noted during a 2-minute observation in conjunction with the behavioral observation. Heart rate and oxygen saturation were also monitored during the study period (Nellcor pulse oximeter, model 395, Tyco Health Care Group LP, Nellcor Puritan Bennett Division, Pleasanton, CA). Additional oxygen requirement (in percentage or liters per minute) was noted at each observation point.
Pain Assessment
Pain was assessed according to the premature infant pain profile (PIPP), a tool that was created to assess short procedural pain 30 seconds after a painful stimulus.20 In the present study, PIPP was also used for evaluating responses from saliva sampling and eye drops (Table 1). An eye examination may last for several minutes, and visibility of the infant's face may be obscured by the examining equipment. In London, where RetCam was used, the PIPP was scored for 30 seconds after the end of the eye examination. In Lund, where indirect ophthalmoscopy was used, the PIPP was scored at maximum response during the eye examination.
Salivary Cortisol
Saliva was collected before the instillation of eye drops, before the eye examination, and at 30 and 60 minutes after the eye examination (Table 1). Salivary cortisol was also sampled at 4 hours after the eye examination in Lund but not in London, because these infants were subjected to blood sampling, according to clinical routines, 1 to 2 hours after the eye examination. Gentle saliva sampling from the inside of the bucca was performed with 2 cotton buds. Because of the existence of components that can disturb the salivary cortisol analysis, the saliva was collected 1 hour after the infant was orally fed. After collection, the saliva was centrifuged, frozen at –20°C, and stored at –70°C. The saliva samples were later analyzed at Linköping University Hospital (Linköping, Sweden). A radioimmunoassay for cortisol was used to analyze cortisol concentrations in saliva. Samples were run in duplicate, and all of the samples from each individual were run in the same assay. Interassay coefficients of variation were 12% at 2.0 nmol/L and 6% at 10.0 nmol/L.21
Ophthalmologist Evaluation
The ROP examinations were mainly performed by 2 ophthalmologists (Drs Fielder and Holm). The ophthalmologists were involved in the study, but neither had previous NIDCAP experience. A brief questionnaire including 4 statements was completed immediately after the eye examination. The ophthalmologists were asked to score the following: (1) how easy the eye examination was to perform (1 = could not be completed, 2 = very difficult, 3 = difficult, 4 = fairly easy, or 5 = very easy); (2) the time the examination took (1 = prolonged, 2 = normal, or 3 = shorter than usual); (3) the nursing care during the examination (1 = hindered, 2 = neither helped nor hindered, or 3 = helped); and (4) a general appreciation of infant distress (1 = very distressed, 2 = fairly distressed, or 3 = not distressed).
Scoring of the Intervention During the Eye Examination
A protocol for quantitative evaluation, that is, the "intervention score," of the support given to the infants was completed immediately after all of the eye examinations. The protocol included 19 items derived from the general guidelines for NIDCAP care (Table 3) that were scored from 1 to 3 (1 = worst or least, 2 = neutral or intermediate, and 3 = best or most): rest between eye drops and eye examination; room and bedside lighting, activity, noise, and bedding during examination; sucking at start, during, and after examination; positioning during examination; approach to examination; delays and interruptions; support during examination; immobilization during examination; facilitated self-regulation using hands during examination; pacing of examination; oxygen during examination; soothing during examination; recovery after examination; and distress experienced by the infant during examination. In London, the assessments were performed by 1 of the NIDCAP-certified persons (Inga Warren, Zoe Khan and Jane Buffery, St Mary's Hospital, London, United Kingdom), and in Lund the scoring was done by Dr Kleberg and/or Ms Berg.
Statistical Analysis
The distribution of data was best suited for nonparametric statistics (Mann-Whitney U test, Spearman correlation, 
2, Wilcoxon); 2-tailed analyses were made using SPSS 12.0 (SPSS Inc, Chicago, IL); a P value <.05 was considered statistically significant. Group comparisons and paired analyses were performed as appropriate. Tests for interrater reliability for ordinal data were determined using Cohen's , which makes adjustment for the agreement expected by chance alone. Mixed linear models were used to evaluate possible confounders on the salivary cortisol responses.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Sixty-eight ROP examinations were evaluated, 33 with NIDCAP interventions and 35 with standard care interventions. The first examination included 36 observations, and the second examination included 32 observations. Four infants did not participate in the second eye examination. In 2 relatively mature infants in London, a second eye examination was not considered necessary. In Lund, 1 fully breastfeeding infant was fed just before the second examination, and another infant was excluded because the eye examination interfered with a medically complicated course and need for surgery (Fig 1).
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NIDCAP Care Versus Standard Care
Behavioral Observation and Pain Assessment (PIPP)
When comparing NIDCAP care and standard care before and after the eye examinations, there were no differences in behavioral scores or PIPP scores (Table 4). However, during the eye examination, the behavioral score was higher (ie, better) for NIDCAP care, although PIPP scores did not differ between the 2 care methods.
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Salivary Cortisol
The results are based on 232 of the 310 saliva samples that were collected. The samples that were not analyzed contained too little saliva to be analyzed (obtaining enough saliva in preterm infants is sometimes a challenge, especially when anticholinergic drugs, ie, the mydriatic eye drops, have been administered). The eye examinations were associated with increased salivary cortisol from baseline, before the eye drops, to 30 and 60 minutes after (P = .043 and 0.001, respectively) with a decrease at 4 hours, although values at this time point were still higher than at baseline (P = .015; paired statistics). There were no differences between baseline values before the eye drops and salivary cortisol 1 hour later, that is, before the eye examinations (P = .898). Consequently, cortisol values just before the eye examination also differed significantly from values at 30 and 60 minutes after the eye examination (P = .007 and .048, respectively). Salivary cortisol decreased between 30 and 60 minutes (P = .053), between 60 minutes and 4 hours (P = .025), and between 30 minutes and 4 hours (P = .002).
During NIDCAP care, but not during standard care, salivary cortisol decreased significantly between 30 and 60 minutes after the eye examinations (P = .017 and .623, respectively). Salivary cortisol also decreased significantly between 30 minutes and 4 hours after the eye examinations during NIDCAP care (P = .008) but not after standard care (P = .092), although between 60 minutes and 4 hours the decrease was almost significant for the standard care (P = .050), indicating a slower return of cortisol after standard care as compared with NIDCAP.
Paired salivary cortisol results were not available for all of the measuring points because of insufficient amounts of saliva, as mentioned above. To include all of the available results, group comparisons were also made on the basis of the interventions. Sixty minutes after the eye examination, salivary cortisol was slightly lower, although not significantly, after NIDCAP care (median [range]: 7.0 nmol/L [0.1–46.3 nmol/L]) versus standard care (median [range]: 11.2 nmol/L [0.8–31.2 nmol/L]; P = .056; Fig 2). There were no significant correlations between any of the salivary cortisol measurements and the infants’ gestational ages, postnatal ages in days, or postmenstrual ages at the examination. However, there were significant correlations between hemoglobin and salivary cortisol at baseline (rs = –0.282; P = .039) and at 60 minutes after the examination (rs = –0.308; P = .037), respectively.
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Heart Rate, Respiration Rate, and Oxygenation
There were no significant differences between the 2 strategies in observed average heart rates, respiratory rates, or oxygen saturation levels before, during, or after the eye examinations. However, oxygen saturation was slightly lower 60 minutes after the eye examination when NIDCAP care was applied (Table 4).
Oxygen Requirement
Oxygen requirements increased after the eye examinations on one third of the occasions, but there were no significant differences between the 2 care strategies.
Intervention Score
The summary of the intervention score differed significantly between standard care, (median [range]: 39 [28–48]) and the NIDCAP intervention (median [range]: 49 [32–53]; P < .001). However, there was a change over time in the amount of support that was provided during standard care (rs = 0.672; P < .001), which gradually increased and approached the score for the NIDCAP intervention (Fig 3). The score for the NIDCAP intervention remained stable over time and did not change with the increasing number of examinations (rs = 0.170; P = .351).
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Ophthalmologist Views
There were no differences in the ophthalmologists’ views of the 2 care strategies. For both the standard care and NIDCAP care the eye examinations were considered "fairly easy" (both methods median scores: 4; ranges: 3–5; P = .674), and the time for examination was "normal" (both methods median scores: 2; ranges: 1–3; P = .325). The nursing care facilitated the examination independent of the type of intervention that was given to the infant (median scores: 3; range of standard care: 2–3; range of NIDCAP care: 1–3; P = .762). The ophthalmologists experienced that the infants were "fairly distressed" (median scores: 2; range of standard care: 1–3: range of NIDCAP care: 2–3; P = .695).
Correlation Between Hemoglobin and Responses During Eye Examination
The median (range) of hemoglobin at the first examination was 116 (81 to 148) g/L and at the second examination was 101 (82 to 132) g/L, and consequently there was a significant correlation between postmenstrual age in weeks at the eye examination and hemoglobin (rs = –0.456; P < .001), although there was no correlation between gestational age at birth and hemoglobin (rs = –0.141; P = .276). There were several significant correlations between hemoglobin and color and between hemoglobin and muscle tone, 2 of the assessments included in the behavioral score. The hemoglobin values correlated significantly with the scores for color at almost all of the evaluation points: baseline (rs = 0.262; P = .055), the response to eye drops (rs = 0.541; P < .001), before the eye examination (rs = 0.267; P = .041), during the eye examination (rs = 0.412, P = .001), 30 minutes after (rs = 0.232; P = .077), 60 minutes after (rs = 0.279; P = .032), and 4 hours after the eye examination (rs = 0.337; P = .036). The hemoglobin levels also correlated with the scores for muscle tone, just before the eye examination and 60 minutes after (rs = 0.396, P = .002 and rs = 0.395, P = .002, respectively). There were no correlations between hemoglobin and heart rates at the various time points.
Comparison Between London and Lund
Hemoglobin values were significantly lower in the infants in London. At the first eye examination, the infants in London had slightly higher postmenstrual age; otherwise, the 2 groups of infants in London and Lund were comparable (Table 2).
Baseline salivary cortisol (before eye drops and before eye examination) was lower in Lund (median [range]: 3.1 nmol/L [0.2–87.1 nmol/L] and 4.0 nmol/L [0.9–33.1 nmol/L]) as compared with London (median [range]: 11.1 nmol/L [5.2–29.6 nmol/L] and 11.8 nmol/L [4.5–50.7 nmol/L]; P < .001 and P = .003, respectively). At 30 minutes after the eye examination, there were no differences between the 2 hospitals, but at 60 minutes, salivary cortisol levels were lower in Lund (P = .003). Figure 4 shows the median salivary cortisol values for the infants at the 2 hospitals.
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Heart rate just before and during the eye examination was higher in London (median [range]: 171 beats per minute [142–196 beats per minute] and 169 beats per minute [144–199 beats per minute], respectively) than in Lund (median [range]: 159 beats per minute [144–185 beats per minute] and 164 beats per minute [119–196 beats per minute] P = .002 and 0.034, respectively). The respiratory rate during the eye examination was also higher in London (median [range]: 93 breaths per minute [72–120 breaths per minute]) than in Lund (median [range]: 70 breaths per minute [30–117 breaths per minute]; P = .027). There were no other differences between infants in the 2 hospitals regarding heart rate, respiratory rate, or oxygen saturation level before, during, or after the eye examinations and no differences in the PIPP scores when evaluating eye drops and saliva sampling. However, the PIPP scores for the eye examinations differed and were higher in Lund (median [range]: 15 [6–18]) versus those in London (median [range]: 9 [0–16]; P < .001). The difference may be attributed to different methods for eye examination or because the PIPP score was evaluated earlier in Lund than in London.
Mixed linear models with log-transformed salivary cortisol values were used to evaluate possible confounders for the salivary cortisol responses. The main factor affecting salivary cortisol was hospital allocation (P = .0001), and hemoglobin, postmenstrual age, and examination order in the study were not significantly associated with salivary cortisol values.
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The present study shows that an NIDCAP intervention during eye examination for ROP reduces stress as indicated by a faster decrease in salivary cortisol after the examination. The eye examinations were associated with an increase in salivary cortisol from baseline to 30 and 60 minutes after the examination. At 30 minutes there were no differences between the 2 care strategies, whereas at 60 minutes there was a significant decrease in salivary cortisol after NIDCAP care. Four hours after the eye examinations, salivary cortisol had further decreased. The behavioral score was also significantly better for NIDCAP care during the eye examination, but not before or after, although this evaluation could not be blinded according to care strategy. There were no differences in PIPP scores, heart rate, respiratory rate, or oxygen saturation level that could be attributed to the interventions. At 60 minutes, however, oxygen saturation was lower in conjunction with NIDCAP care and closer to the recommended oxygen saturation levels for both NICUs. Together these findings indicate that an NIDCAP intervention does not abolish stress and pain responses during ROP examinations in preterm infants, but when infants are subjected to NIDCAP care they seem to recover faster after the examination.
There was a significant change over time, with increasing support given to the infants also during standard care, probably because of the fact that the study procedures were entirely open. The intervention score during NIDCAP care varied but remained stable over time, which was expected, because NIDCAP care is relationship based, and the core concept is to react on infant's signals. Although influences from NIDCAP have been strong in many NICUs, this is the first reported measure of how NIDCAP may influence standard care.
The present study shows that there were some important differences between the 2 groups of infants from London and Lund. The infants had comparable gestational ages, birth weights, and neonatal morbidities, but the infants in London had lower hemoglobin and higher baseline salivary cortisol levels. The decision to collect data on hemoglobin was made before the study, when the investigators discussed possible differences in clinical strategies that could affect the results. The reason for the higher basal salivary cortisol in London is more difficult to explain. It could be because of differences in clinical routines, with the eye examinations scheduled close in time after various care procedures, including diaper change and hand over to the dayshift, as well as differences in the infants’ ethnicity or other environmental factors. Overall baseline salivary cortisol in the current study population, with postnatal ages ranging from 13 to 79 days, seems to be lower than in an intensive care-treated, very preterm population during the first 2 weeks of life.22 The eye examinations in London were performed 1 to 2 hours earlier in the morning than in Lund. In more mature subjects, this could maybe account for the difference in cortisol, with higher levels earlier in the morning. However, this is not likely in the present study population, because the diurnal cortisol rhythm is not developed at 32 to 34 weeks’ postmenstrual age.23 Multicenter studies are often performed without investigating infant baseline characteristics at the different sites. The demonstrated differences, both in baseline characteristics and in responses, between the 2 groups of infants in London and Lund are not only a disadvantage but could be hypothesis generating for future investigations.
Increased awareness of the risks with blood transfusions has restricted the number of transfusions given to very preterm infants. In the present study, a low hemoglobin was associated with lower muscle tone and lower score for skin color but was not otherwise associated with responses in salivary cortisol or PIPP. A lower muscle tone in very preterm infants may imply that the individual has lower strength or energy to react to a noxious stimulus. The PIPP score was not associated with the level of hemoglobin; however, muscle tone is not a part of the PIPP evaluation. There is a potential risk that if the infant has lower muscle tone and reacts less, caregivers may underestimate the infant's signals. Future studies should consider muscle tone when evaluating preterm infants’ reactions to pain and distress that last for longer periods or several minutes, such as during eye examinations. The NIDCAP observation tool assesses infants’ reactions from 3 functional subsystems, autonomic, motor, and state, according to the synactive model.19 The motor system is evaluated from the infants’ muscular tone, as observed in the face, trunk and extremities, and in the extensor and flexor postures, and from spontaneous movements of face, trunk, and extremities. In the present study, standard care was associated with lower muscular tone than NIDCAP care. Holsti et al24 investigated behavioral responses before, during, and after blood collection (including heel lancing and squeezing) and established associations between 8 specific NIDCAP motor behaviors and pain. In the study by Holsti et al,24 flexed arms and legs, extended arms and legs, hand on face, and finger splay increased across the 3 phases before, during, and after the painful stimulus. These authors interpreted finger splay as a developmentally specific cue, because infants who were born at <30 weeks’ gestational age had a higher frequency of finger splays to blood sampling than those who were born 30 gestational weeks. The earlier born infants showed greater finger splay also during baseline evaluation, which was interpreted as a possible display of higher stress levels and a result of "sensitization" from early pain exposure. However, because the infants in the current study were 32 weeks’ PMA at the first examination, we are not sure whether adding "finger splay" in the evaluation has made any difference in the results. In addition, fisting and frowning also increased in response to pain. All of the behaviors, except fisting, returned to baseline 6 minutes after the blood sampling.24 These data were published after the initiation of the current study but could have been valuable to observe. In the present study, fisting was a cue included in the evaluation of muscle tone, although it was not specifically evaluated as a single parameter.
The PIPP is a validated method for measuring procedural pain in preterm infants, and, consequently, this method was chosen for the current evaluation. In the original article by Stevens et al,20 PIPP was scored 30 seconds after a brief noxious stimulus, for example, capillary blood sampling. However, the present data indicate that the PIPP is not an optimal method for evaluating procedures that may last several minutes and with limited possibilities to observe the infants’ faces. This probably explains the lower PIPP scores for the eye examination in London, although it is possible that the different methods for eye examination could also have had an influence. Mehta et al5 demonstrated that infants showed more physiologic and facial expressions of pain during and after examinations using a speculum, which was used with both techniques applied in this study, as compared with examinations without a speculum. The same investigators also reported that the RetCam screening took more time and was associated with more frequent transient desaturations.5 Different studies have used various ways of scoring the PIPP in conjunction with eye examinations. Slevin et al15 did not use PIPP but assessed various responses, including crying times during eye examinations, and noted that infants settled as soon as the eyelid speculum was withdrawn, indicating that the maximum response reflecting pain occurs during the eye examination. Grabska et al14 scored PIPP before, during, and after the eye examination and noted PIPP scores ranging from 4 during baseline to 14 during eye examination, returning to 4 after the eye examination. Boyle et al25 scored PIPP from video recordings but only evaluated the first eye. Their PIPP scores, with pacifier and sucrose intervention, were comparable to the PIPP scores in the current study. These investigators concluded that nonnutritive sucking reduces distress in infants undergoing ROP screening. However, in both the study by Boyle et al25 and in the current study, PIPP scores during the eye examinations remained relatively high despite the interventions. This must be interpreted, because eye examinations are associated with pain and distress despite various interventions to alleviate this, and additional nonpharmacologic and pharmacologic interventions, as well as other methods for eye examination, should be considered.
Several studies evaluating NIDCAP have been performed previously. Fully developed NIDCAP is associated with improved short-term outcomes in morbidity and brain function,26–32 as well as a tendency to enhanced cognitive outcomes, fewer behavioral problems, and better family functioning.26,32–34 In addition, NIDCAP-based interventions during routine care procedures, for example, diaper change and weighing, have also shown positive short-term influences on pain and stress responses.11,12
The current study investigated the effects from a NIDCAP intervention on a single care procedure with the aim of reducing stress and discomfort during a clinical eye examination, a procedure that is well known to cause adverse effects on preterm infants. The results clearly indicate that the NIDCAP intervention succeeded in this aim. The results are even more interesting, because they show that, also in NICUs with partially implemented NIDCAP, a specifically aimed NIDCAP intervention may have additional positive effects on infants. The reason for this is probably the behavioral observation methodology according to NIDCAP, which, in a structured and standardized way, estimates the individual preterm infant's sensitivity and readiness for sensory inputs and assesses the appropriateness and timing of such stimuli. The focus is clearly on the infants’ well-being and needs and not on the timing of clinical routines. The intervention that was developed for the present study was derived from the NIDCAP model and may be applicable to other clinical procedures in the NICU.
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ACKNOWLEDGMENTS |
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The present study was supported by grants from the Swedish Medical Research Council (grant 0037), Lund University, Region Skåne, and county of Östergötland (regional medical research grants).
We are grateful to all of the infants who participated in the study and to all of the nurses in the 2 NICUs who assisted in the study. We would especially like to thank Zoe Khan, RN, and June Buffery, RN, in London and Eva Lantz, RN, and Pia Lundqvist, RN, in Lund.
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FOOTNOTES |
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Accepted Oct 18, 2007.
Address correspondence to Agneta Kleberg, RN, PhD, Neonatal Intensive Care Unit, Department of Pediatrics University Hospital, SE-221 85 Lund, Sweden. E-mail: a.kleberg{at}klemed.se
The authors have indicated they have no financial relationships relevant to this article to disclose.
| What's Known on This Subject Eye examination for retinopathy of prematurity may be distressing and painful. No previous study has investigated effects from a NIDCAP intervention during eye examination.
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| What This Study Adds The study shows that infants recover faster after a NIDCAP intervention, as measured by lower salivary cortisol. Although influences from NIDCAP have been strong in many NICUs this is the first report on how NIDCAP may influence standard care.
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