0
We're unable to sign you in at this time. Please try again in a few minutes.
Retry
We were able to sign you in, but your subscription(s) could not be found. Please try again in a few minutes.
Retry
There may be a problem with your account. Please contact the AMA Service Center to resolve this issue.
Contact the AMA Service Center:
Telephone: 1 (800) 262-2350 or 1 (312) 670-7827  *   Email: subscriptions@jamanetwork.com
Error Message ......
Article |

Kangaroo Care Is Effective in Diminishing Pain Response in Preterm Neonates FREE

C. Celeste Johnston, DEd, RN; Bonnie Stevens, PhD, RN; Janet Pinelli, DNS, RN; Sharyn Gibbins, PhD, RN; Francoise Filion, MS, RN; Anne Jack, MS, RN; Susan Steele, RN; Kristina Boyer, MSc(A), RN; Annie Veilleux, MD
[+] Author Affiliations

From the School of Nursing, McGill University (Dr Johnston, Mr Filion, and Ms Boyer), and the Department of Neonatology, Hopital Sainte Justine (Dr Veilleux), Montreal, Quebec; Faculty Nursing, University of Toronto (Dr Stevens and Ms Jack), the Department of Nursing, Hospital for Sick Children (Dr Stevens and Ms Boyer), and Sunnybrook and Women's College Health Sciences Centre (Dr Gibbins), Toronto, Ontario; and Department of Neonatology, McMaster University, Hamilton, Ontario (Dr Pinelli and Ms Steele).


Arch Pediatr Adolesc Med. 2003;157(11):1084-1088. doi:10.1001/archpedi.157.11.1084.
Text Size: A A A
Published online

Objective  To test the efficacy of maternal skin-to-skin contact, or kangaroo care (KC), on diminishing the pain response of preterm neonates to heel lancing.

Design  A crossover design was used, in which the neonates served as their own controls.

Subjects  Preterm neonates (n = 74), between 32 and 36 weeks' postmenstrual age and within 10 days of birth, who were breathing without assistance and who were not receiving sedatives or analgesics in 3 level II to III neonatal intensive care units in Canada.

Interventions  In the experimental condition, the neonate was held in KC for 30 minutes before the heel-lancing procedure and remained in KC for the duration of the procedure. In the control condition, the neonate was in the prone position in the isolette. The ordering of conditions was random.

Main Outcome Measures  The primary outcome was the Premature Infant Pain Profile, which is composed of 3 facial actions, maximum heart rate, and minimum oxygen saturation changes from baseline in 30-second blocks. Videotapes, taken with the camera positioned on the neonate's face so that an observer could not tell whether the neonate was being held or was in the isolette, were coded by research assistants who were naïve to the purpose of the study. Heart rate and oxygen levels were continuously monitored into a computer for later analysis. A repeated-measures analysis of covariance was used, with order of condition and site as factors and severity of illness as a covariate.

Results  Premature Infant Pain Profile scores across the first 90 seconds from the heel-lancing procedure were significantly (.002<P<.04) lower by 2 points in the KC condition.

Conclusions  For preterm neonates who are 32 weeks' postmenstrual age or older, KC seems to effectively decrease pain from heel lancing. Further study is needed to determine if younger neonates or those requiring assistance in breathing, or older infants or toddlers, would benefit from KC, or if it would remain effective over several procedures. Given its effectiveness, and that parents of neonates in critical care units want to participate more in comforting their children, KC is a potentially beneficial strategy for promoting family health.

Figures in this Article

SKIN-TO-SKIN HOLDING of a newborn, or kangaroo care (KC), named such because of its similarity to marsupial behavior in early life, is gaining acceptance as a standard of care in neonatal intensive care units (NICUs) throughout the world. Findings from a recent survey1 on holding policy in 215 NICUs in the United States indicated that almost three quarters (73%) allowed parents to hold their extubated neonate in KC. First developed as a method of providing warmth for low-birth-weight neonates, KC originated in Bogota, Columbia, in 1979.2 During KC, a diaper-clad neonate is held upright, at an angle of approximately 60°, between the mother's breasts or on the father's chest, providing maximal skin-to-skin contact between neonate and parent.

Kangaroo care has had positive effects on autonomic behavior and state. The state dimension of neurobehavioral organization involves the preterm neonate's ability to make smooth transitions between the sleep, quiet, and awake phases, and to maintain the most desirable state of quiet sleep.3 Several studies48 have shown that 1 to 3 hours spent in KC resulted in increased frequency of quiet sleep, longer duration of quiet sleep, and decreased crying. Preterm neonates of 25 to 36 weeks' gestational age, given unlimited access to KC during their NICU stay, cried less at the age of 6 months than control neonates who did not receive skin-to-skin contact.9

Neonates born prematurely who spend the first weeks of their lives in NICUs undergo many invasive procedures (an average of 2-3 per day, up to 8-10 per day) without benefit of analgesia.1012 Heel lancing is the most common procedure.11,12 There is increasing evidence1317 to suggest that these repeated invasive procedures have long-term consequences. Given the frequency of painful procedures, the potential negative consequences of experiencing repeated painful procedures, and the potential risks of opiate analgesics for frequent procedural pain,18 it would seem that nonpharmacological interventions should be tested to control for procedural pain.19 Pain decreases state regulation,20 and KC has been shown to improve state regulation.3 Sleep state has been associated with decreased pain response,21,22 and KC increases the amount of time in the sleep state.8 Thus, it would seem logical to hypothesize that KC could decrease pain from procedures in neonates. Furthermore, there are reports2326 that mothers of neonates in the NICU are unhappy with pain management and want to participate in comforting their neonates.

One report27 of KC being used with full-term neonates for decreasing pain response during heel lancing showed KC having a powerful effect. In that study, 30 full-term neonates were randomly assigned to KC or swaddled in bassinets to undergo the heel-lancing procedure for routine blood sampling. Crying was reduced by 82% and grimacing by 64% in the KC group vs the control group; also, the heart rate (HR) increased by 8 to 10 beats per minute (bpm) in the KC group vs 36 to 38 bpm in the control group. Based on that study of full-term neonates, we proposed using KC as an intervention for pain in preterm neonates; thus, this study tests the effectiveness of KC response to heel lancing in preterm neonates aged between 32 and 36 weeks' postmenstrual age (pma).

The protocol and consent forms were reviewed by the constituted institutional review board of each participating center. Mothers and their preterm neonates were eligible for participation in the study if the neonates met the following criteria: born between 32 07 and 36 67 completed weeks pma, determined by early ultrasonography at 16 weeks; had informed parental consent; had Apgar scores of greater than 6 at 5 minutes; were within 10 days of birth; were breathing unassisted; did not have any major congenital anomalies; had not experienced a grade III or IV intraventricular hemorrhage or subsequent periventricular leukomalacia; had not undergone surgery; and were not receiving paralytic, analgesic, or sedative medications within 48 hours of study sessions. Mothers had to be willing and able to hold their neonate in the KC position for the study. For practical purposes, if the neonate was to be discharged from the hospital before needing 2 sessions of blood work, the parents were not approached to participate in the study. Using data from an earlier study28 using our primary outcome with a mean difference of 2 points and an SD of 3.5 points, the sample size for a power of 0.8 and a significance level set at .05 was 67.

By using a single-blind crossover design, each neonate was to undergo heel lancing for blood procurement for clinical purposes in either the KC position or the usual cot situation within 4 days of each other. Ordering of conditions was determined randomly by a computer-generated program in the study center. There was a minimum of 24 hours and a maximum of 7 days between conditions, because the frequency of blood sampling was determined by clinical considerations. In the KC condition, the diaper-clad neonate was held upright, at an angle of approximately 60°, between the mother's breasts, providing maximal skin-to-skin contact between the neonate and the mother. A blanket was placed over the neonate's back and the mother's clothes were wrapped around the neonate. The neonate remained in this condition 30 minutes before the heel-lancing procedure. We asked that the mother keep her hands clasped behind the neonate's back throughout the procedure and refrain from touching the neonate's head with her face and from vocalizing to the neonate during the filming (to keep observers blind). In the isolette control condition, the neonate was placed in the isolette in a prone position, swaddled with a blanket (with heel accessible), for 30 minutes before the heel-lancing procedure. The prone position was selected because it controlled for the positional component of KC, allowing us to test the maternal proximity component, and because it is recommended for neonates who are premature.29,30

The heel-lancing procedure was selected as the pain stimulus for several reasons: (1) it is the most common tissue-damaging procedure that premature neonates undergo, (2) the procedure can be relatively standardized across times and staff, and (3) it is an event that occurs as part of routine care of premature neonates and is not an artificial stimulus. The same person conducted the procedure at each site. The procedure includes 5 phases: baseline (5 minutes), heel warming (1 minute), heel lancing with a spring-loaded lancet (Tenderfoot) (15 seconds), heel squeeze (30 seconds of rhythmic squeezing for each block of time, until all required blood is procured), and return to baseline (5 minutes). There was continuous videotaping and pulse oximeter monitoring of the neonate throughout the procedure, which always occurred in the morning. The continuous data were averaged for each block of time.

The primary outcome was the Premature Infant Pain Profile (PIPP).31 The PIPP is a composite measure of pain, including physiological and behavioral indicators that were originally developed using 4 data sets of preterm neonates in a pain/no pain situation. The components are HR, oxygen saturation, 3 facial actions, neurobehavioral state, and pma. Increases in HR are scored in incremental blocks of 5 bpm, ranging from 0 (0-4 bpm) to 3 (≥15 bpm); decreases in oxygen saturation are scored in increments of 2%, ranging from 0 (<2% change) to 3 (≥6% change); and each facial action is scored in increments of a third of the time that the action is seen, from 0 (less than one third of the time) to 3 (all the time). Weights are added for being young (<28 weeks receives a score of 3) and state (quiet sleep receives a score of 3). The scores are totaled, so that with the 7 components, scores can range from 0 to 21. In earlier studies,28 a mean difference of 2 was found (eg, when comparing sucrose with pacifier intervention vs the control condition in neonates aged 28-36 weeks' pma). In studies32,33 of children using a 10-point scale, a change of 1 point (ie, 10%) was reported as clinically important to the children, so that a difference in PIPP scores of 2 points between conditions can be considered clinically important.34 The PIPP has been tested for reliability, construct validity, and clinical utility, all with good results.35 It takes into account the influencing factors of pma and baseline sleep/wake state, shown to contribute to pain response.21,36,37 Internal consistency ranges from 0.59 to 0.76, and interrater and intrarater reliabilities are 0.89 or higher.27

Heart rate and transcutaneous oxygen saturation data were collected via infrared oximeter placed on the unaffected foot of the neonate and connected to a 200- or 3000-pulse oximeter (Nellcor), with a sampling rate of 100 Hz averaged on a second-to-second basis. The HR and oxygen data were fed into a computer (Pentium) via software (Satmaster; EMG Scientific, Beverly Hills, Calif) that keeps track of real time with the physiological data, allows any number of events to be marked, and notes artifacts.

The 3 facial actions (brow bulge, eye squeeze, and nasolabial furrow) of the PIPP were continuously recorded by a digital camera (model KS162; Panasonic) that allows for close-range high-quality facial images. The camera was in close-up focus on the neonate's face, with little surrounding area, no sound, and minimal color, and turned 60° in the KC condition so as to decrease the possibility of unblinding by research assistants who scored the tapes. Research assistants, who were blinded to the purpose of the study by being told that the study was about neonatal facial actions, coded facial actions in the laboratory of the principal investigator (C.C.J.). These assistants were students from outside the department, and they conducted the coding in laboratory space reserved only for themselves or others involved so that there was minimal exposure to discussion about the study. At the conclusion of the study, they were asked what they thought the study was about and they said that they thought it had to do with pain and possibly development. Facial actions were scored according to the Neonatal Facial Coding System,21 which provides a detailed, anatomically based, and objective description of newborns' reactions to the heel-lancing procedure. The selected facial actions were scored on a second-to-second basis. The tapes were played back in real time on a video monitor (model AG-1970; Panasonic) with stop-frame capability and clock to the fourth decimal place. Each recording session was scored 3 times, once for each of the facial actions, using a laptop computer with software developed in the laboratory that records the scores and allows for information on artifacts to be included. A final score, based on percentage of time the action was present, was calculated for the block time of interest. The neurobehavioral state component was determined according to Prechtl38 categories of quiet sleep or quiet awake or active sleep or active awake during baseline. Age (pma) was taken from the medical record, based on early ultrasonography at 16 weeks.

Severity of illness, as a potentially confounding variable, was scored using the Score for Neonatal Acute Physiology (SNAP-II)39; for the 12-hour period after birth and for the 24 hours before the procedure, the SNAP-II–Perinatal Extension was used.39 The elements for this score can be found in the medical record, and include hemodynamic, respiratory, hematologic, metabolic, electrolytic, and neurologic variables. The score has predictive validity for perinatal mortality.39

Across the 3 sites, there were 502 neonates admitted during the data collection period (April 9, 2001, to June 28, 2002). Most neonates did not meet the age criteria; of those who did meet the age criteria, 8 were to be discharged from the hospital within 48 hours, 3 were considered too ill, and 1 mother was infected. Of the 502 neonates, 172 met the selection criteria and were approached, and 108 agreed to participate. The main reason for refusal was that the parents did not want their child involved in any research (n = 11). Other reasons for refusal were that the mother was too ill (n = 4), the family lived too far to come in (n = 4), the neonate would associate the mother with pain (n = 3), too many things were going on to handle anything else (n = 3), the parents did not understand French or English well enough (n = 2), the parents were too busy with other children at home (n = 2), the parents did not want to do KC (n = 2), the father refused and the mother deferred (n = 2), the parents did not want to be filmed (n = 1), and the mother did not want the neonate to cry on her (n = 1). For the remainder, no reason was given. Physiological and behavioral data were completed for KC and control sessions for 74 neonates. The main reasons that neonates were not included were that the neonate was discharged from the unit (n = 25), the neonate did not require blood work within the time frame of the study (n = 6), or there was equipment failure (n = 3). The 74 neonates remaining in the study were a mean age of 33.7 weeks (SD, 1.1 weeks; range, 32.0-36.0 weeks), at birth weighed a mean of 2054 g (SD, 406 g; range, 1320-3125 g), and were generally in a state of good health (mean SNAP-II–Perinatal Extension, 6.7; SD, 9.4; range, 0-39). Of the 74 neonates, 41 (55%) were boys, 40 (54%) had a score of 0 on the severity of illness measure, and only 6 (8%) were in the second risk category (of 5 categories). There were no significant differences between those who remained in the hospital for both sessions and those who were discharged from the hospital or did not require blood work (mean age, 33.8 weeks [P = .66]; mean birth weight, 2110 g [P = .17]; mean SNAP-II–Perinatal Extension, 6.1 [P = .76]). No neonate had to be removed from KC because of physiological instability.

A repeated-measures analysis of covariance, with condition (KC vs isolette) as the repeated factor, order of conditions and site as additional factors, and severity of illness as a covariate, was conducted for each 30-second period following heel lancing through 2 minutes, when most (52 [70%] of 74) procedures had been completed. There were equal instances of KC and isolette conditions in the remaining time. Thirty-four neonates underwent KC before the isolette condition. There were no significant effects for site (P = .29) or order (P = .54) of condition, and severity of illness (SNAP-II and SNAP-II–Perinatal Extension) was not significant (P = .19). There were no significant differences in heart rate (P = .72) or oxygen saturation (P = .11) at baseline, although 62 infants (84%) in the KC condition were in quiet sleep in the isolette condition (χ23 = 65.56, P = .000). All facial actions were 0 during baseline. Pain scores (PIPP) were significantly lower in the KC condition at 30 seconds (difference, 1.5 points; P = .04), 60 seconds (difference, 2.2 points; P = .002), and 90 seconds (difference, 1.8 points; P = .02), but not at 120 seconds (difference, 0.6 point; P = .37), after the heel-lancing procedure (Table 1). When examined individually, HR and oxygen saturation were similar in both conditions, but the facial actions contributed significantly (.000<P<.005) to the total pain score, with facial actions on average 20% greater in the control vs the KC condition (Figure 1).

Table Graphic Jump LocationThe PIPP Scores in 74 Neonates Following Heel Lancing
Place holder to copy figure label and caption

Facial actions contributed significantly (.000<P<.005) to the total pain score, with facial actions on average 20% greater in the isolette (control) group vs the group who received kangaroo care (KC).

Graphic Jump Location

It seems that maternal contact in the skin-to-skin paradigm of KC is an analgesic for preterm neonates between 32 and 36 weeks' pma who are undergoing heel lancing for blood procurement. As well as statistically significant differences, the magnitude of the difference in scores between the isolette and KC conditions can also be considered clinically important.34 The differences between isolette and KC were approximately between 1.5 and 2.2 in the first three 30-second blocks, of a total possible score of 21; thus, there was close to a 10% difference. A similar finding of the efficacy of KC for reducing procedural pain was shown earlier in full-term neonates,27 but, to our knowledge, has not previously been shown in preterm neonates. The mechanisms could be related to state regulation, which has been reported to be a result of KC.48 Maternal touch is implicated in development, and has been demonstrated in humans and animals.4043 Maternal influence has had a dampening effect on pain response in animal studies.44,45 It could also be the neonate's recognition of the mother and that the presence of familiar stimuli was comforting. In animal studies,4648 it has been shown that endorphins are released on reunion with a mother following a separation. In full-term neonates, it has been shown that neonates recognize their mother's voice,49,50 and breast milk is thought to smell similar to amniotic fluid,5153 so that the neonates may have recognized their mothers through olfactory and auditory senses. This sensory memory could take place earlier than 40 weeks' gestation.50,54,55 More research is needed to understand the mechanisms of analgesia provided by maternal presence in neonates born before their due date.

There could have been some influence of position on the ability of the technicians who obtained blood to do so. The technicians reported that obtaining blood from neonates in the KC condition was more difficult than obtaining blood from neonates prone in the isolette. Therefore, if positioning had influenced the results because of facility for blood sampling, it would likely have been in the opposite direction. This may have contributed to the modest difference between conditions.

Mothers who agreed to participate in this study are mothers who were comfortable in the KC situation in a busy NICU. This could represent a selection bias in that mothers who were not as comfortable may not have been as effective in providing comfort to their neonates. Some mothers expressed concern about the potential risk of negative conditioning if KC was used repeatedly for painful procedures. In one study36 that followed up neonates weekly for changes in their pain expression, a sham heel-lancing procedure, which included warming, was performed; from the age of 28 to 36 weeks, there was no indication of conditioning to associate heel warming with the impending lancing. More recently, Goubet et al56 reported evidence of conditioning to heel lancing when the technician lifted the heel and held it. The increase in HR they reported could be attributed to handling, not anticipation, of heel lancing. Taddio et al31 reported response to alcohol swabbing in full-term neonates who had undergone numerous blood samplings because of their mother's diabetes mellitus compared with neonates who had not undergone heel lancing. This is evidence of conditioning, but alcohol swabbing is a noxious stimulus, whereas being held in the KC condition is not noxious, as noted by the increased incidence of the quiet state during baseline in the KC condition vs the isolette. Comfort in distressed states is a basic maternal role, and we are unaware of any reports of neonates forming negative associations to their mothers in the context of providing comfort during a painful event.

Further study is needed to determine which groups within the NICU can benefit from this intervention. The neonates in the study were generally healthy, but perhaps even younger, smaller, and ventilated neonates could benefit.57 Given a refusal rate of close to 40% and mothers' spontaneous expressions of concern, research into maternal attitudes on their role in relieving pain would be informative. Given that the prevalence of KC in North American NICUs1 is high and the number of invasive procedures, especially heel-lancing procedures, is high,10,11 based on even this single study, it would seem appropriate to offer the option of KC to mothers who want to provide comfort for a heel-lancing procedure to their stable neonate older than 32 weeks' pma.

Corresponding author: C. Celeste Johnston, DEd, RN, School of Nursing, McGill University, 3506 University St, Montreal, Quebec, Canada H3A 2A7 (e-mail: celeste.johnston@mcgill.ca).

Accepted for publication December 31, 2002.

This study was supported by grant MOP 38074 from the Canadian Institutes of Health Research, Ottawa, Ontario.

We thank the neonates, parents, and staff of the NICUs at Hopital Sainte Justine, Montreal, Quebec; McMaster Children's Hospital, Hamilton, Ontario; and Sunnybrook and Women's College Health Sciences Centre, Toronto, Ontario.

What This Study Adds

The salient components of KC that are thought to promote quiet state and release endorphins are closeness, warmth, and rhythmic breathing of the mother (which provides vestibular stimulation). Kangaroo care has been shown to have analgesic effects on full-term neonates; however, before this study, it was unknown whether it would have the same effect on preterm neonates, who are less developed in state regulation.

Kangaroo care was effective in significantly decreasing pain response on the behavioral components of a validated composite measure of pain in preterm neonates. Given the many invasive procedures that are part of clinical care in preterm neonates, KC may be a safe analgesic alternative in neonates in whom it is feasible and with mothers who are comfortable providing KC for painful events.

Franck  LSBernal  HGale  G Infant holding policies and practices in neonatal units. Neonatal Netw. 2002;2113- 20
PubMed Link to Article
Whitelaw  ASleath  K Myth of the marsupial mother: home care of very low birth weight babies in Bogota, Colombia. Lancet. 1985;11206- 1208
PubMed Link to Article
Ludington-Hoe  SMSwinth  JY Developmental aspects of kangaroo care. J Obstet Gynecol Neonatal Nurs. 1996;25691- 703
PubMed Link to Article
deLeeuw  RColin  EMDunnebier  EAMirmiran  M Physiologic effects of kangaroo care in very small preterm infants. Biol Neonate. 1991;59149- 155
PubMed Link to Article
Ludington-Hoe  SMHashemi  MSArgote  LAMedellin  GRey  H Selected physiologic measures and behavior during paternal skin contact with Colombian preterm infants. J Dev Physiol. 1992;18223- 232
PubMed
Ludington-Hoe  SMNguyen  NSwinth  JYSatyshur  RD Kangaroo care compared to incubators in maintaining body warmth in preterm infants. Biol Res Nurs. 2000;260- 73
PubMed Link to Article
Ludington  SMAndersen  GCSwinth  JThompson  CHadeed  AJ Kangaroo care. Neonatal Netw. 1994;1361- 62
PubMed
Ludington  SM Energy conservation during skin-to-skin contact between premature infants and their mothers. Heart Lung. 1990;19 ((pt 1)) 445- 451
PubMed
Whitelaw  AHeisterkamp  GSleath  KAcolet  DRichards  M Skin to skin contact for very low birthweight infants and their mothers. Arch Dis Child. 1988;631377- 1381
PubMed Link to Article
Anand  KJSelankio  JDfor the SOPAIN Study Group, Routine analgesia practices in 109 neonatal intensive care units (NICU's) [abstract]. Pediatr Res. 1996;39 ((special issue)) 192A
Link to Article
Johnston  CCCollinge  JMHenderson  SAnand  KJS A cross sectional survey of pain and analgesia in Canadian neonatal intensive care units. Clin J Pain. 1997;131- 5
PubMed Link to Article
Barker  DPRutter  N Exposure to invasive procedures in neonatal intensive care unit admissions. Arch Dis Child Fetal Neonatal Ed. 1995;72F47- F48
PubMed Link to Article
Anand  KJScalzo  FM Can adverse neonatal experiences alter brain development and subsequent behavior? Biol Neonate. 2000;7769- 82
PubMed Link to Article
Anand  KJ Effects of perinatal pain and stress. Prog Brain Res. 2000;122117- 129
PubMed
Grunau  REOberlander  TFWhitfield  MFFitzgerald  CLee  SK Demographic and therapeutic determinants of pain reactivity in very low birth weight neonates at 32 weeks' postconceptional age. Pediatrics. 2001;107105- 112
PubMed Link to Article
Grunau  REAnand  KJS, Stevens BJ, McGrath PJ, eds.ed Long-term consequences of pain in human neonates. Pain in Neonates. 2nd ed. Amsterdam, the Netherlands Elsevier Science Publishers2000;55- 76
Johnston  CCStevens  BJ Experience in a neonatal intensive care unit affects pain response. Pediatrics. 1996;98925- 930
PubMed
Marsh  DFHatch  DJFitzgerald  M Opioid systems and the newborn. Br J Anaesth. 1997;79787- 795
PubMed Link to Article
Stevens  BGibbins  SFranck  LS Treatment of pain in the neonatal intensive care unit. Pediatr Clin North Am. 2000;47633- 650
PubMed Link to Article
Grossman  RGLawhon  GAnand  KJS, McGrath PJ, eds.ed Individualized supportive care to reduce pain and stress. Pain in Neonates. Amsterdam, the Netherlands Elsevier Science Publishers1993;233- 254
Grunau  RVECraig  KD Pain expression in neonates: facial action and cry. Pain. 1987;28395- 410
PubMed Link to Article
Stevens  BJJohnston  CC Physiological responses of premature infants to a painful stimulus. Nurs Res. 1994;43226- 231
PubMed Link to Article
Franck  LSScurr  KCouture  S Parent views of infant pain and pain management in the neonatal intensive care unit. Newborn Infant Nurs Rev. 2001;1106- 113
Link to Article
Lucey  JF Parent dissatisfaction with neonatal intensive care unit care and suggestions for improvements. Pediatrics. 1993;92724
PubMed
Miles  MSFunk  SGCarlson  J Parental Stressor Scale: neonatal intensive care unit. Nurs Res. 1993;42148- 152
PubMed Link to Article
Miles  MSFunk  SGKasper  MA The neonatal intensive care unit environment: sources of stress for parents. AACN Clin Issues Crit Care Nurs. 1991;2346- 354
PubMed
Gray  LWatt  LBlass  EM Skin-to-skin contact is analgesic in healthy newborns. Pediatrics. 2000;105e14Available athttp://www.pediatrics.org/cgi/content/full/105/1/e14Accessed March 7, 2003
PubMed Link to Article
Stevens  BJJohnston  CFranck  LPetryshen  PJack  AFoster  R The efficacy of developmentally sensitive interventions and sucrose for relieving procedural pain in very low birth weight neonates. Nurs Res. 1999;4835- 43
PubMed Link to Article
Baird  TMPaton  JBFisher  DE Improved oxygenation with prone positioning in neonates: stability of increased transcutaneous Po2. J Perinatol. 1991;11315- 318
PubMed
Martin  RJDiFiore  JMKorenke  CBRandal  HMiller  MJBrooks  LJ Vulnerability of respiratory control in healthy preterm infants placed supine. J Pediatr. 1995;127609- 614
PubMed Link to Article
Taddio  AShah  VGilbert-MacLeod  CKatz  J Conditioning and hyperalgesia in newborns exposed to repeated heel lances. JAMA. 2002;288857- 861
PubMed Link to Article
Bullock  B Pediatric emergency department assessment of clinically significant and important changes in acute pain [abstract]. Pediatr Res. 2001;49 ((special issue)) 86A
Powell  CVKelly  AMWilliams  A Determining the minimum clinically significant difference in visual analog pain score for children. Ann Emerg Med. 2001;3728- 31
PubMed Link to Article
Stevens  BGibbins  S Clinical utility and clinical significance in the assessment and management of pain in vulnerable infants. Clin Perinatol. 2002;29459- 468
PubMed Link to Article
Ballantyne  MStevens  BMcAllister  MDionne  KJack  A Validation of the Premature Infant Pain Profile in the clinical setting. Clin J Pain. 1999;15297- 303
PubMed Link to Article
Johnston  CCStevens  BJYang  FHorton  L Developmental changes in response to heelstick by premature infants: a prospective cohort study. Dev Med Child Neurol. 1996;38438- 445
PubMed Link to Article
Stevens  BJJohnston  CCHorton  L Factors that influence the behavioral pain responses of premature infants. Pain. 1994;59101- 109
PubMed Link to Article
Prechtl  HFR The behavioral states of the newborn infant: a review. Brain Res. 1974;76185- 212
PubMed Link to Article
Richardson  DKCorcoran  JDEscobar  GJLee  SK SNAP-II and SNAPPE-II: simplified newborn illness severity and mortality risk scores. J Pediatr. 2001;13892- 100
PubMed Link to Article
Fleming  ASO'Day  DHKraemer  GW Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations. Neurosci Biobehav Rev. 1999;23673- 685
PubMed Link to Article
Kuhn  CMSchanberg  SM Responses to maternal separation: mechanisms and mediators. Int J Dev Neurosci. 1998;16261- 270
PubMed Link to Article
Weiss  SJWilson  PSeed  MSPaul  SM Early tactile experience of low birth weight children: links to later mental health and social adaptation. Infant Child Dev. 2001;1093- 115
Link to Article
Liu  DDiorio  JDay  JCFrancis  DDMeaney  MJ Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci. 2000;3799- 806
PubMed Link to Article
Blass  EMShide  DJZaw-Mon  CSorrentino  J Mother as shield: differential effects of contact and nursing on pain responsivity in infant rats—evidence for nonopioid mediation. Behav Neurosci. 1995;109342- 353
PubMed Link to Article
Walker  CDKudreikis  KSherrard  AJohnston  CC Repeated neonatal pain influences maternal behavior, but not stress responsiveness in rat offspring. Brain Res Dev Brain Res. 2003;140253- 261
PubMed Link to Article
Carden  SEBarr  GAHofer  MA Differential effects of specific opioid receptor agonists on rat pup isolation cells. Brain Res Dev Brain Res. 1991;6217- 22
PubMed Link to Article
Carden  SEHofer  MA Socially mediated reduction of isolation distress in rat pups is blocked by naltrexone but not by Ro 15-1788. Behav Neurosci. 1990;104457- 463
PubMed Link to Article
Kalin  NHShelton  SELynn  DE Opiate systems in mother and infant primates coordinate intimate contact during reunion. Psychoneuroendocrinology. 1995;20735- 742
PubMed Link to Article
DeCasper  AJFifer  WP Of human bonding: newborns prefer their mothers' voices. Science. 1980;2081174- 1176
PubMed Link to Article
DeCasper  AJSpence  MJ Prenatal maternal speech influences newborn's perception of speech sounds. Infant Behav Dev. 1986;9133- 150
Link to Article
Porter  RHWinberg  J Unique salience of maternal breast odors for newborn infants. Neurosci Biobehav Rev. 1999;23439- 449
PubMed Link to Article
Varendi  HPorter  RHWinberg  J Attractiveness of amniotic fluid odor: evidence of prenatal olfactory learning? Acta Paediatr. 1996;851223- 1227
PubMed Link to Article
Varendi  HPorter  RH Breast odour as the only maternal stimulus elicits crawling towards the odour source. Acta Paediatr. 2001;90372- 375
PubMed Link to Article
DeCasper  AJLecanuet  JPBusnel  MCGranier-Deferre  CMaugeais  R Fetal reactions to recurrent maternal speech. Infant Behav Dev. 1994;17159- 164
Link to Article
Ockleford  EMVince  MALayton  CReader  MR Response of neonates to parents' and others' voices. Early Hum Dev. 1988;1827- 36
PubMed Link to Article
Goubet  NClifton  RKShah  B Learning about pain in preterm newborns. J Dev Behav Pediatr. 2001;22418- 424
PubMed Link to Article
Clifford  PABarnsteiner  J Kangaroo care and the very low birthweight infant: is it an appropriate practice for all premature babies? J Neonatal Nurs. 2001;714- 18

Figures

Place holder to copy figure label and caption

Facial actions contributed significantly (.000<P<.005) to the total pain score, with facial actions on average 20% greater in the isolette (control) group vs the group who received kangaroo care (KC).

Graphic Jump Location

Tables

Table Graphic Jump LocationThe PIPP Scores in 74 Neonates Following Heel Lancing

References

Franck  LSBernal  HGale  G Infant holding policies and practices in neonatal units. Neonatal Netw. 2002;2113- 20
PubMed Link to Article
Whitelaw  ASleath  K Myth of the marsupial mother: home care of very low birth weight babies in Bogota, Colombia. Lancet. 1985;11206- 1208
PubMed Link to Article
Ludington-Hoe  SMSwinth  JY Developmental aspects of kangaroo care. J Obstet Gynecol Neonatal Nurs. 1996;25691- 703
PubMed Link to Article
deLeeuw  RColin  EMDunnebier  EAMirmiran  M Physiologic effects of kangaroo care in very small preterm infants. Biol Neonate. 1991;59149- 155
PubMed Link to Article
Ludington-Hoe  SMHashemi  MSArgote  LAMedellin  GRey  H Selected physiologic measures and behavior during paternal skin contact with Colombian preterm infants. J Dev Physiol. 1992;18223- 232
PubMed
Ludington-Hoe  SMNguyen  NSwinth  JYSatyshur  RD Kangaroo care compared to incubators in maintaining body warmth in preterm infants. Biol Res Nurs. 2000;260- 73
PubMed Link to Article
Ludington  SMAndersen  GCSwinth  JThompson  CHadeed  AJ Kangaroo care. Neonatal Netw. 1994;1361- 62
PubMed
Ludington  SM Energy conservation during skin-to-skin contact between premature infants and their mothers. Heart Lung. 1990;19 ((pt 1)) 445- 451
PubMed
Whitelaw  AHeisterkamp  GSleath  KAcolet  DRichards  M Skin to skin contact for very low birthweight infants and their mothers. Arch Dis Child. 1988;631377- 1381
PubMed Link to Article
Anand  KJSelankio  JDfor the SOPAIN Study Group, Routine analgesia practices in 109 neonatal intensive care units (NICU's) [abstract]. Pediatr Res. 1996;39 ((special issue)) 192A
Link to Article
Johnston  CCCollinge  JMHenderson  SAnand  KJS A cross sectional survey of pain and analgesia in Canadian neonatal intensive care units. Clin J Pain. 1997;131- 5
PubMed Link to Article
Barker  DPRutter  N Exposure to invasive procedures in neonatal intensive care unit admissions. Arch Dis Child Fetal Neonatal Ed. 1995;72F47- F48
PubMed Link to Article
Anand  KJScalzo  FM Can adverse neonatal experiences alter brain development and subsequent behavior? Biol Neonate. 2000;7769- 82
PubMed Link to Article
Anand  KJ Effects of perinatal pain and stress. Prog Brain Res. 2000;122117- 129
PubMed
Grunau  REOberlander  TFWhitfield  MFFitzgerald  CLee  SK Demographic and therapeutic determinants of pain reactivity in very low birth weight neonates at 32 weeks' postconceptional age. Pediatrics. 2001;107105- 112
PubMed Link to Article
Grunau  REAnand  KJS, Stevens BJ, McGrath PJ, eds.ed Long-term consequences of pain in human neonates. Pain in Neonates. 2nd ed. Amsterdam, the Netherlands Elsevier Science Publishers2000;55- 76
Johnston  CCStevens  BJ Experience in a neonatal intensive care unit affects pain response. Pediatrics. 1996;98925- 930
PubMed
Marsh  DFHatch  DJFitzgerald  M Opioid systems and the newborn. Br J Anaesth. 1997;79787- 795
PubMed Link to Article
Stevens  BGibbins  SFranck  LS Treatment of pain in the neonatal intensive care unit. Pediatr Clin North Am. 2000;47633- 650
PubMed Link to Article
Grossman  RGLawhon  GAnand  KJS, McGrath PJ, eds.ed Individualized supportive care to reduce pain and stress. Pain in Neonates. Amsterdam, the Netherlands Elsevier Science Publishers1993;233- 254
Grunau  RVECraig  KD Pain expression in neonates: facial action and cry. Pain. 1987;28395- 410
PubMed Link to Article
Stevens  BJJohnston  CC Physiological responses of premature infants to a painful stimulus. Nurs Res. 1994;43226- 231
PubMed Link to Article
Franck  LSScurr  KCouture  S Parent views of infant pain and pain management in the neonatal intensive care unit. Newborn Infant Nurs Rev. 2001;1106- 113
Link to Article
Lucey  JF Parent dissatisfaction with neonatal intensive care unit care and suggestions for improvements. Pediatrics. 1993;92724
PubMed
Miles  MSFunk  SGCarlson  J Parental Stressor Scale: neonatal intensive care unit. Nurs Res. 1993;42148- 152
PubMed Link to Article
Miles  MSFunk  SGKasper  MA The neonatal intensive care unit environment: sources of stress for parents. AACN Clin Issues Crit Care Nurs. 1991;2346- 354
PubMed
Gray  LWatt  LBlass  EM Skin-to-skin contact is analgesic in healthy newborns. Pediatrics. 2000;105e14Available athttp://www.pediatrics.org/cgi/content/full/105/1/e14Accessed March 7, 2003
PubMed Link to Article
Stevens  BJJohnston  CFranck  LPetryshen  PJack  AFoster  R The efficacy of developmentally sensitive interventions and sucrose for relieving procedural pain in very low birth weight neonates. Nurs Res. 1999;4835- 43
PubMed Link to Article
Baird  TMPaton  JBFisher  DE Improved oxygenation with prone positioning in neonates: stability of increased transcutaneous Po2. J Perinatol. 1991;11315- 318
PubMed
Martin  RJDiFiore  JMKorenke  CBRandal  HMiller  MJBrooks  LJ Vulnerability of respiratory control in healthy preterm infants placed supine. J Pediatr. 1995;127609- 614
PubMed Link to Article
Taddio  AShah  VGilbert-MacLeod  CKatz  J Conditioning and hyperalgesia in newborns exposed to repeated heel lances. JAMA. 2002;288857- 861
PubMed Link to Article
Bullock  B Pediatric emergency department assessment of clinically significant and important changes in acute pain [abstract]. Pediatr Res. 2001;49 ((special issue)) 86A
Powell  CVKelly  AMWilliams  A Determining the minimum clinically significant difference in visual analog pain score for children. Ann Emerg Med. 2001;3728- 31
PubMed Link to Article
Stevens  BGibbins  S Clinical utility and clinical significance in the assessment and management of pain in vulnerable infants. Clin Perinatol. 2002;29459- 468
PubMed Link to Article
Ballantyne  MStevens  BMcAllister  MDionne  KJack  A Validation of the Premature Infant Pain Profile in the clinical setting. Clin J Pain. 1999;15297- 303
PubMed Link to Article
Johnston  CCStevens  BJYang  FHorton  L Developmental changes in response to heelstick by premature infants: a prospective cohort study. Dev Med Child Neurol. 1996;38438- 445
PubMed Link to Article
Stevens  BJJohnston  CCHorton  L Factors that influence the behavioral pain responses of premature infants. Pain. 1994;59101- 109
PubMed Link to Article
Prechtl  HFR The behavioral states of the newborn infant: a review. Brain Res. 1974;76185- 212
PubMed Link to Article
Richardson  DKCorcoran  JDEscobar  GJLee  SK SNAP-II and SNAPPE-II: simplified newborn illness severity and mortality risk scores. J Pediatr. 2001;13892- 100
PubMed Link to Article
Fleming  ASO'Day  DHKraemer  GW Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations. Neurosci Biobehav Rev. 1999;23673- 685
PubMed Link to Article
Kuhn  CMSchanberg  SM Responses to maternal separation: mechanisms and mediators. Int J Dev Neurosci. 1998;16261- 270
PubMed Link to Article
Weiss  SJWilson  PSeed  MSPaul  SM Early tactile experience of low birth weight children: links to later mental health and social adaptation. Infant Child Dev. 2001;1093- 115
Link to Article
Liu  DDiorio  JDay  JCFrancis  DDMeaney  MJ Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci. 2000;3799- 806
PubMed Link to Article
Blass  EMShide  DJZaw-Mon  CSorrentino  J Mother as shield: differential effects of contact and nursing on pain responsivity in infant rats—evidence for nonopioid mediation. Behav Neurosci. 1995;109342- 353
PubMed Link to Article
Walker  CDKudreikis  KSherrard  AJohnston  CC Repeated neonatal pain influences maternal behavior, but not stress responsiveness in rat offspring. Brain Res Dev Brain Res. 2003;140253- 261
PubMed Link to Article
Carden  SEBarr  GAHofer  MA Differential effects of specific opioid receptor agonists on rat pup isolation cells. Brain Res Dev Brain Res. 1991;6217- 22
PubMed Link to Article
Carden  SEHofer  MA Socially mediated reduction of isolation distress in rat pups is blocked by naltrexone but not by Ro 15-1788. Behav Neurosci. 1990;104457- 463
PubMed Link to Article
Kalin  NHShelton  SELynn  DE Opiate systems in mother and infant primates coordinate intimate contact during reunion. Psychoneuroendocrinology. 1995;20735- 742
PubMed Link to Article
DeCasper  AJFifer  WP Of human bonding: newborns prefer their mothers' voices. Science. 1980;2081174- 1176
PubMed Link to Article
DeCasper  AJSpence  MJ Prenatal maternal speech influences newborn's perception of speech sounds. Infant Behav Dev. 1986;9133- 150
Link to Article
Porter  RHWinberg  J Unique salience of maternal breast odors for newborn infants. Neurosci Biobehav Rev. 1999;23439- 449
PubMed Link to Article
Varendi  HPorter  RHWinberg  J Attractiveness of amniotic fluid odor: evidence of prenatal olfactory learning? Acta Paediatr. 1996;851223- 1227
PubMed Link to Article
Varendi  HPorter  RH Breast odour as the only maternal stimulus elicits crawling towards the odour source. Acta Paediatr. 2001;90372- 375
PubMed Link to Article
DeCasper  AJLecanuet  JPBusnel  MCGranier-Deferre  CMaugeais  R Fetal reactions to recurrent maternal speech. Infant Behav Dev. 1994;17159- 164
Link to Article
Ockleford  EMVince  MALayton  CReader  MR Response of neonates to parents' and others' voices. Early Hum Dev. 1988;1827- 36
PubMed Link to Article
Goubet  NClifton  RKShah  B Learning about pain in preterm newborns. J Dev Behav Pediatr. 2001;22418- 424
PubMed Link to Article
Clifford  PABarnsteiner  J Kangaroo care and the very low birthweight infant: is it an appropriate practice for all premature babies? J Neonatal Nurs. 2001;714- 18

Correspondence

CME
Meets CME requirements for:
Browse CME for all U.S. States
Accreditation Information
The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
Note: You must get at least of the answers correct to pass this quiz.
You have not filled in all the answers to complete this quiz
The following questions were not answered:
Sorry, you have unsuccessfully completed this CME quiz with a score of
The following questions were not answered correctly:
Commitment to Change (optional):
Indicate what change(s) you will implement in your practice, if any, based on this CME course.
Your quiz results:
The filled radio buttons indicate your responses. The preferred responses are highlighted
For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.
Submit a Comment

Multimedia

Some tools below are only available to our subscribers or users with an online account.

Web of Science® Times Cited: 105

Related Content

Customize your page view by dragging & repositioning the boxes below.

Articles Related By Topic
Related Collections