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Journal for Specialists in Pediatric Nursing
ORIGINAL ARTICLE
Relationship between energy expenditure and stress behaviors of preterm infants in the neonatal intensive care unit Hung-Chih Lin, Li-Chi Huang, Tsai-Chung Li, Chau-Huei Chen, Jean Bachman, and Niang-Huei Peng Hung-Chih Lin, MD, is Professor, Department of Medicine, China Medical University, and Chief, Division of Neonatology, China Medical University Hospital; Li-Chi Huang, EdD, RN, is Associate Professor, School of Nursing, China Medical University, and Adjunct Educational Supervisor, Nursing Department, China Medical University Hospital; Tsai-Chung Li, PhD, is Professor, Graduate Institution of Biostatistics, China Medical University; Chau-Huei Chen, MD, is Director, Center for Faculty Development, Taichung Veterans General Hospital, Taichung, Taiwan; Jean Bachman, DNS, RN, is Associate Professor, College of Nursing, University of Missouri—St. Louis, St. Louis, Missouri, USA; and Niang-Huei Peng, PhD, RN, is Assistant Professor, Nursing College, Central Taiwan University of Science and Technology, Taichung, Taiwan
Search terms Behaviors, energy expenditure, nursing intervention, preterm infant. Author contact lilyfl[email protected], with a copy to the Editor: [email protected] Disclosure: The authors report no actual or potential conflicts of interest. First Received February 18, 2014; Revision received July 23, 2014; Accepted for publication July 24, 2014. doi: 10.1111/jspn.12087
Abstract Purpose. This research evaluated the relationship between behaviors and energy expenditure in preterm infants receiving nursing interventions. Design and Methods. This study was an explorative secondary data analysis from a previous study. The current study investigated energy expenditure calculated using heart rate-based energy expenditure-estimate across 500 repeated measures for 37 infants. Results. Research results indicate that preterm infants expend more energy when they show the following seven behaviors: grimace, sucking, diffusion squirm, fist, gape face, salute, and sneezing. Practice Implications. The interventions for preterm infants should be flexible, according to the infant’s stress behaviors and conditions of energy expenditure.
The preterm infant is not simply smaller than the full-term newborn. Preterm infants have many physiological limitations because of immaturity of all major systems, forcing them to rely on sophisticated medical technologies and intensive nursing interventions for survival before they reach developmental maturity (Farrell, Inturrisi, Bergman, Kenner, & Howell, 2003). Unfortunately, preterm infants are especially vulnerable to inadequate growth because of low energy reserves (Denne, 2001; Grenier, Bigsby, Vergara, & Lester, 2003; Hulzebos & Sauer, 2007). Compared with full-term infants, preterm infants need more energy for physiologic energy growth and development (Neal & Lindeke, 2008). Energy expenditure is the other part of the energy balance equation and is the summation of its multiple components. Energy output can be divided into energy lost in excretions plus metabolizable energy (Denne, 2001). Metabolizable energy is divided into total energy expenditure (TEE) and energy stored in growth (Hulzebos & Sauer, 2007). In preterm infants, the major compoJournal for Specialists in Pediatric Nursing 19 (2014) 331–338 © 2014, Wiley Periodicals, Inc.
nent of TEE is near the resting metabolic rate (Denne, 2001; Hulzebos & Sauer, 2007). Several studies have demonstrated that the varied, sometimes noxious, stimuli received by preterm infants in the neonatal intensive care unit (NICU) may increase energy expenditure during this medically critical time (Als, 2007; Guilfoy, Wright-Coltart, Leitch, & Denne, 2008; Leitch & Denne, 2000). Although preterm infants are dependent upon intensive care interventions for survival, they are also vulnerable to the effects of these same interventions. Preterm infants in the NICU often receive interventions that combine multiple stimuli, including sound, light, tactile stimulation, and pain (Bremmer, Byers, & Kieble, 2003; Holditch-Davis, Blackburn, & VandenBerg, 2003). Preterm infants’ responses to caregiving and interventions, such as auscultation, venipuncture, suctioning, and positioning changes, increase expenditure of their already very limited energy reserves (Bremmer et al., 2003; Valentin, Francisb, & Shaul, 2007). Several researchers have proposed that altering 331
Relationship Between Energy Expenditure and Stress Behaviors of Preterm Infants in the Neonatal Intensive Care Unit
caregiving patterns may help better conserve energy in preterm infants (Als, 2007; Peng et al., 2009; Valentin et al., 2007). Neonatal clinicians must monitor the stress responses and energy expenditure of their patients and moderate accordingly the stimuli resulting from interventions. Neonatal stress increases energy expenditure and may affect the outcomes of healing, recovery from illness, and growth (Als, 2007; Bauer, Maier, Hellstern, & Linderkamp, 2003; Hulzebos & Sauer, 2007). Behavioral cues are routinely used to monitor infants’ stress levels (Epstein, 2005; Harrison, Roane, & Weaver, 2004; Peng et al., 2009). Behaviors are infants’ only means of communicating their needs and responses to their environment (Als, 2007; Holditch-Davis et al., 2003), and they may be closely correlated to increasing energy expenditure during periods of environmental stress (Peng et al., 2011; Valentin et al., 2007; VandenBerg, 2007). However, there is little research to validate this assumption. It is therefore important to simultaneously examine both energy expenditure and stress behavioral indicators of infants receiving nursing interventions. RESEARCH PURPOSE
The aim of this study was to evaluate the relationship between behaviors and energy expenditure in preterm infants receiving nursing interventions in the NICU. RESEARCH METHODS
This study was an explorative secondary data analysis from a previous study examining the relationships between physiological stress signals and behavioral stress responses in one group of preterm infants using a prospective repeated-measure design (Peng et al., 2011). Participants and setting
A convenience sample of 37 preterm infants was observed during periods of environmental stress in NICUs at two medical centers from 2007 to 2008. All infants were born at less than 37 weeks’ gestational age (GA) and, at the time of study, were less than 28 days of age, and were in an incubator. The research sample excluded preterm infants with major health complications, a congenital anomaly, or a need for surgery. Preterm infants who were using mechanical ventilation (i.e., intermittent positive pressure ventilation and high-frequency ventilation), photo332
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therapy, and sedative medicines also were excluded from this research (Peng et al., 2011). Data collection
In the original study, research variables were measured every 2 min during four 60-min observation periods conducted over two research days. There were 4,164 repeated recordings in the original study (Peng et al., 2009). In this investigation, we used only the data recorded while the preterm infants received nursing interventions for a total of 500 measurements. According to the literature (Fielder & Moseley, 2000; Nair, Gupta, & Jatana, 2003), neonatal nursing interventions often have an all-or-nothing quality, ranging from no contact to repeated, frequent, stressful, and often painful interventions (Holditch-Davis et al., 2003). These interventions often also combine multiple stimuli, including sound, light, tactile touch, and pain (Bremmer et al., 2003). Therefore, we classified different neonatal interventions into five levels based on accompanying levels of discomfort (Peng et al., 2009). The nursing interventions were classified into five levels: level 1: interventions that include noise or light stimulation; level 2: interventions that include both noise and light stimulation; level 3: interventions that include noise or light and handling stimulation; level 4: interventions that include noise, light, and handling stimulation; and level 5: any intervention that causes pain. A phonometer and a photometer were used to measure the noise and light levels during nursing interventions in the previous study. The nursing interventions were recorded and classified into one of these five levels by a research nurse. Thirty-one specific behaviors were scored by observation of the preterm infants every 2 min during research time. These stress behavioral responses included six stress behaviors related to sleep–wake states (hypoalert, hyperalert, gaze averting, upward gaze, staring, and grimace), eight selfregulatory behaviors (hand clasp, hand to mouth, foot clasp, holding on, leg brace, sucking, tuck trunk, and balance motor tone), and 14 stress behaviors (arch, diffusion squirm, finger splay, fisting, gape face, salute, sitting-on-air, stretch down, tongue extension, tremor, startle, twitch, yawning, and sneezing). The operational definitions of the specific behaviors were based on previous studies (Peng et al., 2011). To facilitate detailed coding of the behavioral variables, the infants were videotaped Journal for Specialists in Pediatric Nursing 19 (2014) 331–338 © 2014, Wiley Periodicals, Inc.
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Relationship Between Energy Expenditure and Stress Behaviors of Preterm Infants in the Neonatal Intensive Care Unit
during each observation, and measures of research behaviors were coded from videotapes. The heart rate-based energy expenditure estimate (HR-based EE-estimate) was used to estimate the TEE of the preterm infants (Yu et al., 2012). HR monitoring, or HR-based EE-estimate, is the described energy expenditure estimation method and is based on a well-known relationship between cardiorespiratory function and measured energy expenditure (Firstbeat Technologies Ltd, 2007). According to research (Chessex et al., 1981), preterm infants expend more energy when their HR drops below 120 beats/min or exceeds 140 beats/ min. The energy expenditure of the preterm infants was calculated by the following equation (Chessex et al., 1981):
Energy expenditure per heart beat (cal kg × beat ) mean metabolic rate × duration of study ( min ) ; = accumulated heart beats Y = −.0000291X 3 + .01685X 2 − 2.93X + 197 (Y = metabolic rate ; X = heart beats ) RELIABILITY AND VALIDITY
The reliability and validity tests of the measurements of physiological signals, specific behaviors in preterm infants and nursing interventions, were conducted in the original research (Peng et al., 2011). The validity and reliability of HR-based EE-estimate has been verified against reference methods (Beghin et al., 2000, 2002; Chessex et al., 1981) and whole-body indirect calorimetry (Brage et al., 2007; Perring, Henderson, & Cooke, 2000; Pierro, Jones, Hammond, Donnell, & Lloyd, 1994). Moreover, researchers have defined the relationship between HR and metabolic rate in newborn infants and evaluated the accuracy of prediction of metabolic rate from HR (Beghin et al., 2000; Pinelli & Symington, 2005). The reliability and validity of the research equation has been evidenced by Chessex et al. (1981) and other researchers (Beghin et al., 2000). Ethical considerations
The Institutional Review Board of the Taichung Veterans General Hospital approved the study protocol for this secondary analysis. For the original study, the Institutional Review Board of the University of Missouri—St. Louis and research hospitals in central Taiwan approved the study protocol and written parental consent was obtained (Peng et al., 2009). Journal for Specialists in Pediatric Nursing 19 (2014) 331–338 © 2014, Wiley Periodicals, Inc.
Data analysis
Multiple linear regressions of generalized estimating equations (GEEs) were used to examine the relationships between energy expenditure and special behaviors during periods of exposure to nursing interventions. All analyses were done by SPSS 19.0 for Window (SPSS Inc., Chicago, IL., USA). A p-value of < .05 was considered as statistically significant. RESULTS Descriptions of research variables
Research data comprised 500 repeated-measure recordings from 37 preterm infants receiving nursing interventions that included diaper changing, positioning, heel sticks, and physical assessments. The research data are described in Table 1. A baseline measure of light (mean = .324 foot-candles [ft-c]) and sound (mean = 52.56 decibels [dB]) was recorded 3,664 times when no intervention was occurring. The range of light illumination was .94–2.3 ft-c, and the range of sound was 56.12–63.62 dB during periods of nursing interventions. The mean energy expenditure was 39.32 cal/kg (SD = 2.78), and range of energy expenditure was 36.91–62.7 cal/kg. Relationships between behaviors and changes in energy expenditure
The GEE models were used to examine the correlation between energy expenditure and stress behavioral responses in preterm infants. After multivariate adjustment of the effects of time and nursing interventions, there were statistically significant increasing relationships between different levels of energy expenditure and seven stress behavioral responses, including grimace, sucking, diffusion squirm, fist, gape face, salute, and sneezing (Table 2). The odds ratio of the presence of these behaviors increased with respect to the energy expenditure. Table 1. Description of Research Data (N = 37; Female = 18, Male = 19; 500 Repeated-Measure Recordings) Characteristics
Mean
SD
Range
Gestational age (GA; weeks) 32.05 2.208 27–36 Birth body weight (BBW; g) 1662.35 8.373 890.00–2655.00 1 min APGAR score 6.616 2.043 1–9 5 min APGAR score 8.054 1.311 5–10 1673.24 327.707 890–2655 Body weight (BW; g)a Initial study age (days) 10.648 8.373 1–27 (days) Note: aBody weight: the body weight on the research day. AGPAR, appearance, pulse rate, reflex irritability, activity, and respiratory effort.
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Table 2. Relationships Between Behaviors and Changes in Energy Expenditure Variables
Odds ratio
Standard error
Grimace Intercept .272 8.873 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 2.262 1.210 Nursing interventions (nursing interventions level 0 as reference) Level 1, 2 4.162 1.259 Level 3, 4, 5 4.670 1.348 GA .966 1.080 Age (days) .953 1.018 BBW .999 1.001 BW 1.001 1.001 Sucking Intercept .025 45.428 Nursing interventions (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 2.397 1.295 Environmental stress (level 0 as reference) Level 1, 2 2.549 1.289 Level 3, 4, 5 3.634 1.546 GA 1.032 1.153 Age (days) .997 1.022 BBW .999 1.001 BW 1.001 1.001 Diffusion squirm Intercept .123 3.596 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 1.567 1.165 Nursing interventions (level 0 as reference) Level 1, 2 1.451 1.237 Level 3, 4, 5 1.337 1.293 GA 1.020 1.041 Age (days) .987 1.010 BBW 1.000 1.000 BW 1.000 1.001 Fist Intercept .329 15.252 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 1.892 1.321 Nursing interventions (level 0 as reference) Level 1, 2 1.089 1.511 Level 3, 4, 5 1.789 1.463 GA .923 1.097 Age .984 1.024 BBW .999 1.001 BW 1.000 1.001 Gape face Intercept .392 10.464 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 2.477 1.524 Nursing interventions (level 0 as reference) Level 1, 2 3.264 1.460 Level 3, 4, 5 10.678 1.504 GA .822 1.097 Age .973 1.029 BBW 1.003 1.002 BW .999 1.002
334
95% confidence interval
Z
p value
(.004, 19.627)
−.596
.551
(1.558, 3.284)
4.291
< .001*
(2.649, 6.539) (2.599, 8.389) (.831,1.123) (.921, .987) (.997, 1.000) (.999, 1.003)
6.186 5.156 −.451 −2.702 −1.380 1.063
< .001* < .001* .652 .07 .167 .288
(.000, 43.966)
−.969
.333
(1.444, 3.979)
3.382
.001*
(1.550, 4.191) (1.547, 8.537) (.781, 1.363) (.956, 1.041) (.997, 1.001) (.999, 1.003)
3.687 2.961 .222 −.118 −1.185 .793
< .001* .003* .824 .906 .236 .428
(.010, 1.511)
−1.637
.102
(1.163, 2.112)
2.949
.003*
(.956, 2.203) (.808, 2.214) (.943, 1.103) (.968, 1.007) (.999, 1.001) (.999, 1.001)
1.746 1.130 .494 −1.281 −.634 .183
.081 .258 .621 .2 .526 .855
(.002, 68.551)
−.408
.683
(1.096, 3.264)
2.290
.022*
(.485, 2.444) (.848, 3.772) (.771, 1.106) (.940, 1.031) (.997, 1.002) (.998, 1.003)
.206 1.527 −.867 −.684 −.348 .290
.837 .127 .386 .494 .728 .772
(.004, 39.040)
−.399
.69
(1.085, 5.655)
2.153
.031*
(1.555, 6.852) (4.799, 23.759) (.685, .985) (.921, 1.028) (.999, 1.006) (.995, 1.002)
3.126 5.804 −2.127 −.972 1.431 −.877
.002* < .001* .033 .331 .152 .38
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Table 2. Continued Variables
Odds ratio
Standard error
Salute Intercept .008 15.098 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 1.533 1.228 Nursing interventions (level 0 as reference) Level 1, 2 5.229 1.277 Level 3, 4, 5 3.945 1.313 GA 1.031 1.097 Age .983 1.024 BBW 1.000 1.001 BW 1.000 1.001 Sneezing Intercept .013 2850.629 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 8.457 2.034 Nursing interventions (level 0 as reference) Level 1∼5 .460 2.126 GA .846 1.431 Age .950 1.033 BBW .998 1.002 BW 1.003 1.003
95% confidence interval
Z
(.000,1.706)
−1.763
p value .078
(1.025, 2.292)
2.081
.037*
(3.237, 8.445) (2.313, 6.730) (.861, 1.236) (.938,1.031) (.998, 1.002) (.998, 1.002)
6.762 5.037 .335 −.709 .354 −.109
< .001* < .001* .737 .478 .723 .913
(.000, 75,917.73)
−.547
.584
(2.104, 33.996)
3.008
.003*
−1.029 −.466 −1.563 −.958 1.185
.304 .641 .118 .338 .236
(.105, 2.019) (.419, 1.709) (.891, 1.013) (.995, 1.002) (.998, 1.009)
Note: BBW, birth body weight; BW, body weight; CI, confidence interval; ee, energy expenditure; GA, gestational age; HR, heart rate. *p < .05.
Energy expenditure was positively and significantly associated with grimace (p < .001, adjusted odds ratio: 2.262, 95% confidence interval [CI]: 1.558–3.284), sucking (p = .001, adjusted odds ratio: 2.397, 95% CI: 1.444–3.979), diffusion squirm (p = .003, adjusted odds ratio: 1.567, 95% CI: 1.163– 2.112), fist (p = .022, adjusted odds ratio: 1.892, 95% CI: 1.096–3.264), gape face (p = .031, adjusted odds ratio: 2.477, 95% CI: 1.085–5.655), salute (p = .037, adjusted odds ratio: 1.533, 95% CI: 1.025–2.292), and sneezing (p = .003, adjusted odds ratio: 8.457, 95% CI: 2.104–33.996). After adjustment for the effects of time, GA, birth days, birth body weight, and body weight, there were significantly increasing relationships between different levels of nursing interventions (levels 1–5) and these seven specific behaviors (Table 2). In other words, the odds ratios of these different specific behaviors being present increased with respect to the increase of levels of nursing interventions. DISCUSSION
Grimace is the most common stress behavioral response of infants toward painful stimulations and any other interventions (Mitchell, Brooks, & Roane, 2000). After multivariate adjustment, factors signifiJournal for Specialists in Pediatric Nursing 19 (2014) 331–338 © 2014, Wiley Periodicals, Inc.
cantly associated with grimace were energy expenditure and different levels of nursing intervention. The odds of exhibiting grimace were 2.262 times higher for infants with higher levels of energy expenditure compared with those with lower levels of energy expenditure (Table 2). Based on these results, neonatal caregivers should carefully observe preterm infants’ facial expressions while applying interventions in order to maintain the energy reserves of these infants. In this research, sucking is also positively related to energy expenditure and receiving different nursing interventions (p = .001). Infants with higher levels of energy expenditure were more likely to show sucking than those with lower levels of energy expenditure while receiving different interventions. However, a previous study (Ernst et al., 1989) demonstrated no effect on energy expenditure. Pinelli and Symington (2005) also made the same statement based on their literature reviews and meta-analysis. Sucking on a pacifier, nonnutritive sucking, during gavage feeding may improve the digestion of feeding and may also have a calming effect on infants; this is a common self-regulatory behavior of preterm infants suffering environmental stress (Als, 2007; VandenBerg, Browne, Perez, & Newstetter, 2003). Because this study’s method of measuring energy 335
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expenditure differed from that of other studies, further research might be needed into this issue. This research also found significantly positive relationships between energy expenditure and five stress behaviors (diffusion squirm, fist, gape face, salute, and sneezing) in preterm infants. After multivariate adjustment, diffusion squirm was significantly related to energy expenditure (p = .03). The odds of exhibiting diffusion squirm were 1.567 times higher for infants with higher levels of energy expenditure than for those with lower levels of energy expenditure. Similarly, after multivariate adjustment, fist was significantly related to energy expenditure (p = .022). The odds of exhibiting fist were 1.892 times higher for infants with higher levels of energy expenditure than for those with lower levels. After multivariate adjustment, there was a significantly positive relationship between sneezing and increased energy expenditure (p = .03). Infants with higher levels of energy expenditure were more likely to have sneezing than those with lower levels (adjusted odds ratio = 8.457, 95% CI = 2.104–33.996). After multivariate adjustment, factors significantly associated with gape face were energy expenditure and different levels of interventions (p = .031). The odds of exhibiting gape face were 2.477 times higher for infants with higher levels of energy expenditure compared with those with lower levels. Energy expenditure and various interventions were significantly correlated with salute (p = .037). The odds of exhibiting salute were 1.533 times higher for infants with higher levels of energy expenditure compared with those with lower levels. This current study is the first investigation to closely explore the relationships between behavioral stress responses and energy expenditure in preterm infants while they received nursing interventions. Our research findings indicate that preterm infants expend more energy when they show sucking, grimaces, or any of five stress behaviors (diffusion squirm, fist, gape face, salute, and sneezing) while receiving nursing interventions. Several studies have also found an assumption that reducing the need for stress or self-regulatory behaviors in preterm infants may conserve energy for their growth (Hulzebos & Sauer, 2007; Grenier et al., 2003; Guilfoy et al., 2008). Our findings help to verify this assumption. Neonatal clinicians should assess preterm infants’ energy levels and their stress behavioral responses while conducting nursing interventions. 336
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LIMITATIONS
Research methods used in this study may influence the generalizability of the results. The measurement of research data in the original study was recorded every 2 min, which may overlook some important factors affecting stress behaviors and the measurements of energy expenditure. Moreover, the small sample size could produce a significant bias. Most participants were born near 32 weeks GA, which may limit generalizability. Further research should investigate a larger sample size and include infants of different GAs.
How might this information affect nursing practice?
Research findings demonstrated significantly positive correlations between specific behaviors and levels of energy expenditure in preterm infants. Research findings also illuminated the possibility of continuous monitoring of the energy expenditure of preterm infants, which is important for neonatal caregivers wishing to provide quality interventions to their patients. Because of their immature physiological mechanisms, preterm infants are easily overtaxed and show exhausted states while experiencing environmental overstimulation (Als, 2007). Many fragile preterm infants at this critical physiological time are obtunded and show few stress behavioral responses because of low energy levels (Walden, Sudia-Robinson, & Carner, 2001). Although determination of valid measures of stress behavioral cues in preterm infants during nursing interventions is necessary, the amount of their energy expenditure that is available for response should be considered. In order to provide the protective, nurturing interventions that will help preterm infants conserve energy and achieve physiological stability, there is a need for neonatal nurses to understand the energy expenditure of their patients. Based on our research, we strongly suggest that caregiving during this critical medical time should be flexible according to the infant’s physiological needs, indicated by their stress behaviors and conditions of energy expenditure.
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Journal for Specialists in Pediatric Nursing
ORIGINAL ARTICLE
Relationship between energy expenditure and stress behaviors of preterm infants in the neonatal intensive care unit Hung-Chih Lin, Li-Chi Huang, Tsai-Chung Li, Chau-Huei Chen, Jean Bachman, and Niang-Huei Peng Hung-Chih Lin, MD, is Professor, Department of Medicine, China Medical University, and Chief, Division of Neonatology, China Medical University Hospital; Li-Chi Huang, EdD, RN, is Associate Professor, School of Nursing, China Medical University, and Adjunct Educational Supervisor, Nursing Department, China Medical University Hospital; Tsai-Chung Li, PhD, is Professor, Graduate Institution of Biostatistics, China Medical University; Chau-Huei Chen, MD, is Director, Center for Faculty Development, Taichung Veterans General Hospital, Taichung, Taiwan; Jean Bachman, DNS, RN, is Associate Professor, College of Nursing, University of Missouri—St. Louis, St. Louis, Missouri, USA; and Niang-Huei Peng, PhD, RN, is Assistant Professor, Nursing College, Central Taiwan University of Science and Technology, Taichung, Taiwan
Search terms Behaviors, energy expenditure, nursing intervention, preterm infant. Author contact lilyfl[email protected], with a copy to the Editor: [email protected] Disclosure: The authors report no actual or potential conflicts of interest. First Received February 18, 2014; Revision received July 23, 2014; Accepted for publication July 24, 2014. doi: 10.1111/jspn.12087
Abstract Purpose. This research evaluated the relationship between behaviors and energy expenditure in preterm infants receiving nursing interventions. Design and Methods. This study was an explorative secondary data analysis from a previous study. The current study investigated energy expenditure calculated using heart rate-based energy expenditure-estimate across 500 repeated measures for 37 infants. Results. Research results indicate that preterm infants expend more energy when they show the following seven behaviors: grimace, sucking, diffusion squirm, fist, gape face, salute, and sneezing. Practice Implications. The interventions for preterm infants should be flexible, according to the infant’s stress behaviors and conditions of energy expenditure.
The preterm infant is not simply smaller than the full-term newborn. Preterm infants have many physiological limitations because of immaturity of all major systems, forcing them to rely on sophisticated medical technologies and intensive nursing interventions for survival before they reach developmental maturity (Farrell, Inturrisi, Bergman, Kenner, & Howell, 2003). Unfortunately, preterm infants are especially vulnerable to inadequate growth because of low energy reserves (Denne, 2001; Grenier, Bigsby, Vergara, & Lester, 2003; Hulzebos & Sauer, 2007). Compared with full-term infants, preterm infants need more energy for physiologic energy growth and development (Neal & Lindeke, 2008). Energy expenditure is the other part of the energy balance equation and is the summation of its multiple components. Energy output can be divided into energy lost in excretions plus metabolizable energy (Denne, 2001). Metabolizable energy is divided into total energy expenditure (TEE) and energy stored in growth (Hulzebos & Sauer, 2007). In preterm infants, the major compoJournal for Specialists in Pediatric Nursing 19 (2014) 331–338 © 2014, Wiley Periodicals, Inc.
nent of TEE is near the resting metabolic rate (Denne, 2001; Hulzebos & Sauer, 2007). Several studies have demonstrated that the varied, sometimes noxious, stimuli received by preterm infants in the neonatal intensive care unit (NICU) may increase energy expenditure during this medically critical time (Als, 2007; Guilfoy, Wright-Coltart, Leitch, & Denne, 2008; Leitch & Denne, 2000). Although preterm infants are dependent upon intensive care interventions for survival, they are also vulnerable to the effects of these same interventions. Preterm infants in the NICU often receive interventions that combine multiple stimuli, including sound, light, tactile stimulation, and pain (Bremmer, Byers, & Kieble, 2003; Holditch-Davis, Blackburn, & VandenBerg, 2003). Preterm infants’ responses to caregiving and interventions, such as auscultation, venipuncture, suctioning, and positioning changes, increase expenditure of their already very limited energy reserves (Bremmer et al., 2003; Valentin, Francisb, & Shaul, 2007). Several researchers have proposed that altering 331
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caregiving patterns may help better conserve energy in preterm infants (Als, 2007; Peng et al., 2009; Valentin et al., 2007). Neonatal clinicians must monitor the stress responses and energy expenditure of their patients and moderate accordingly the stimuli resulting from interventions. Neonatal stress increases energy expenditure and may affect the outcomes of healing, recovery from illness, and growth (Als, 2007; Bauer, Maier, Hellstern, & Linderkamp, 2003; Hulzebos & Sauer, 2007). Behavioral cues are routinely used to monitor infants’ stress levels (Epstein, 2005; Harrison, Roane, & Weaver, 2004; Peng et al., 2009). Behaviors are infants’ only means of communicating their needs and responses to their environment (Als, 2007; Holditch-Davis et al., 2003), and they may be closely correlated to increasing energy expenditure during periods of environmental stress (Peng et al., 2011; Valentin et al., 2007; VandenBerg, 2007). However, there is little research to validate this assumption. It is therefore important to simultaneously examine both energy expenditure and stress behavioral indicators of infants receiving nursing interventions. RESEARCH PURPOSE
The aim of this study was to evaluate the relationship between behaviors and energy expenditure in preterm infants receiving nursing interventions in the NICU. RESEARCH METHODS
This study was an explorative secondary data analysis from a previous study examining the relationships between physiological stress signals and behavioral stress responses in one group of preterm infants using a prospective repeated-measure design (Peng et al., 2011). Participants and setting
A convenience sample of 37 preterm infants was observed during periods of environmental stress in NICUs at two medical centers from 2007 to 2008. All infants were born at less than 37 weeks’ gestational age (GA) and, at the time of study, were less than 28 days of age, and were in an incubator. The research sample excluded preterm infants with major health complications, a congenital anomaly, or a need for surgery. Preterm infants who were using mechanical ventilation (i.e., intermittent positive pressure ventilation and high-frequency ventilation), photo332
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therapy, and sedative medicines also were excluded from this research (Peng et al., 2011). Data collection
In the original study, research variables were measured every 2 min during four 60-min observation periods conducted over two research days. There were 4,164 repeated recordings in the original study (Peng et al., 2009). In this investigation, we used only the data recorded while the preterm infants received nursing interventions for a total of 500 measurements. According to the literature (Fielder & Moseley, 2000; Nair, Gupta, & Jatana, 2003), neonatal nursing interventions often have an all-or-nothing quality, ranging from no contact to repeated, frequent, stressful, and often painful interventions (Holditch-Davis et al., 2003). These interventions often also combine multiple stimuli, including sound, light, tactile touch, and pain (Bremmer et al., 2003). Therefore, we classified different neonatal interventions into five levels based on accompanying levels of discomfort (Peng et al., 2009). The nursing interventions were classified into five levels: level 1: interventions that include noise or light stimulation; level 2: interventions that include both noise and light stimulation; level 3: interventions that include noise or light and handling stimulation; level 4: interventions that include noise, light, and handling stimulation; and level 5: any intervention that causes pain. A phonometer and a photometer were used to measure the noise and light levels during nursing interventions in the previous study. The nursing interventions were recorded and classified into one of these five levels by a research nurse. Thirty-one specific behaviors were scored by observation of the preterm infants every 2 min during research time. These stress behavioral responses included six stress behaviors related to sleep–wake states (hypoalert, hyperalert, gaze averting, upward gaze, staring, and grimace), eight selfregulatory behaviors (hand clasp, hand to mouth, foot clasp, holding on, leg brace, sucking, tuck trunk, and balance motor tone), and 14 stress behaviors (arch, diffusion squirm, finger splay, fisting, gape face, salute, sitting-on-air, stretch down, tongue extension, tremor, startle, twitch, yawning, and sneezing). The operational definitions of the specific behaviors were based on previous studies (Peng et al., 2011). To facilitate detailed coding of the behavioral variables, the infants were videotaped Journal for Specialists in Pediatric Nursing 19 (2014) 331–338 © 2014, Wiley Periodicals, Inc.
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during each observation, and measures of research behaviors were coded from videotapes. The heart rate-based energy expenditure estimate (HR-based EE-estimate) was used to estimate the TEE of the preterm infants (Yu et al., 2012). HR monitoring, or HR-based EE-estimate, is the described energy expenditure estimation method and is based on a well-known relationship between cardiorespiratory function and measured energy expenditure (Firstbeat Technologies Ltd, 2007). According to research (Chessex et al., 1981), preterm infants expend more energy when their HR drops below 120 beats/min or exceeds 140 beats/ min. The energy expenditure of the preterm infants was calculated by the following equation (Chessex et al., 1981):
Energy expenditure per heart beat (cal kg × beat ) mean metabolic rate × duration of study ( min ) ; = accumulated heart beats Y = −.0000291X 3 + .01685X 2 − 2.93X + 197 (Y = metabolic rate ; X = heart beats ) RELIABILITY AND VALIDITY
The reliability and validity tests of the measurements of physiological signals, specific behaviors in preterm infants and nursing interventions, were conducted in the original research (Peng et al., 2011). The validity and reliability of HR-based EE-estimate has been verified against reference methods (Beghin et al., 2000, 2002; Chessex et al., 1981) and whole-body indirect calorimetry (Brage et al., 2007; Perring, Henderson, & Cooke, 2000; Pierro, Jones, Hammond, Donnell, & Lloyd, 1994). Moreover, researchers have defined the relationship between HR and metabolic rate in newborn infants and evaluated the accuracy of prediction of metabolic rate from HR (Beghin et al., 2000; Pinelli & Symington, 2005). The reliability and validity of the research equation has been evidenced by Chessex et al. (1981) and other researchers (Beghin et al., 2000). Ethical considerations
The Institutional Review Board of the Taichung Veterans General Hospital approved the study protocol for this secondary analysis. For the original study, the Institutional Review Board of the University of Missouri—St. Louis and research hospitals in central Taiwan approved the study protocol and written parental consent was obtained (Peng et al., 2009). Journal for Specialists in Pediatric Nursing 19 (2014) 331–338 © 2014, Wiley Periodicals, Inc.
Data analysis
Multiple linear regressions of generalized estimating equations (GEEs) were used to examine the relationships between energy expenditure and special behaviors during periods of exposure to nursing interventions. All analyses were done by SPSS 19.0 for Window (SPSS Inc., Chicago, IL., USA). A p-value of < .05 was considered as statistically significant. RESULTS Descriptions of research variables
Research data comprised 500 repeated-measure recordings from 37 preterm infants receiving nursing interventions that included diaper changing, positioning, heel sticks, and physical assessments. The research data are described in Table 1. A baseline measure of light (mean = .324 foot-candles [ft-c]) and sound (mean = 52.56 decibels [dB]) was recorded 3,664 times when no intervention was occurring. The range of light illumination was .94–2.3 ft-c, and the range of sound was 56.12–63.62 dB during periods of nursing interventions. The mean energy expenditure was 39.32 cal/kg (SD = 2.78), and range of energy expenditure was 36.91–62.7 cal/kg. Relationships between behaviors and changes in energy expenditure
The GEE models were used to examine the correlation between energy expenditure and stress behavioral responses in preterm infants. After multivariate adjustment of the effects of time and nursing interventions, there were statistically significant increasing relationships between different levels of energy expenditure and seven stress behavioral responses, including grimace, sucking, diffusion squirm, fist, gape face, salute, and sneezing (Table 2). The odds ratio of the presence of these behaviors increased with respect to the energy expenditure. Table 1. Description of Research Data (N = 37; Female = 18, Male = 19; 500 Repeated-Measure Recordings) Characteristics
Mean
SD
Range
Gestational age (GA; weeks) 32.05 2.208 27–36 Birth body weight (BBW; g) 1662.35 8.373 890.00–2655.00 1 min APGAR score 6.616 2.043 1–9 5 min APGAR score 8.054 1.311 5–10 1673.24 327.707 890–2655 Body weight (BW; g)a Initial study age (days) 10.648 8.373 1–27 (days) Note: aBody weight: the body weight on the research day. AGPAR, appearance, pulse rate, reflex irritability, activity, and respiratory effort.
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Table 2. Relationships Between Behaviors and Changes in Energy Expenditure Variables
Odds ratio
Standard error
Grimace Intercept .272 8.873 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 2.262 1.210 Nursing interventions (nursing interventions level 0 as reference) Level 1, 2 4.162 1.259 Level 3, 4, 5 4.670 1.348 GA .966 1.080 Age (days) .953 1.018 BBW .999 1.001 BW 1.001 1.001 Sucking Intercept .025 45.428 Nursing interventions (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 2.397 1.295 Environmental stress (level 0 as reference) Level 1, 2 2.549 1.289 Level 3, 4, 5 3.634 1.546 GA 1.032 1.153 Age (days) .997 1.022 BBW .999 1.001 BW 1.001 1.001 Diffusion squirm Intercept .123 3.596 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 1.567 1.165 Nursing interventions (level 0 as reference) Level 1, 2 1.451 1.237 Level 3, 4, 5 1.337 1.293 GA 1.020 1.041 Age (days) .987 1.010 BBW 1.000 1.000 BW 1.000 1.001 Fist Intercept .329 15.252 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 1.892 1.321 Nursing interventions (level 0 as reference) Level 1, 2 1.089 1.511 Level 3, 4, 5 1.789 1.463 GA .923 1.097 Age .984 1.024 BBW .999 1.001 BW 1.000 1.001 Gape face Intercept .392 10.464 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 2.477 1.524 Nursing interventions (level 0 as reference) Level 1, 2 3.264 1.460 Level 3, 4, 5 10.678 1.504 GA .822 1.097 Age .973 1.029 BBW 1.003 1.002 BW .999 1.002
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95% confidence interval
Z
p value
(.004, 19.627)
−.596
.551
(1.558, 3.284)
4.291
< .001*
(2.649, 6.539) (2.599, 8.389) (.831,1.123) (.921, .987) (.997, 1.000) (.999, 1.003)
6.186 5.156 −.451 −2.702 −1.380 1.063
< .001* < .001* .652 .07 .167 .288
(.000, 43.966)
−.969
.333
(1.444, 3.979)
3.382
.001*
(1.550, 4.191) (1.547, 8.537) (.781, 1.363) (.956, 1.041) (.997, 1.001) (.999, 1.003)
3.687 2.961 .222 −.118 −1.185 .793
< .001* .003* .824 .906 .236 .428
(.010, 1.511)
−1.637
.102
(1.163, 2.112)
2.949
.003*
(.956, 2.203) (.808, 2.214) (.943, 1.103) (.968, 1.007) (.999, 1.001) (.999, 1.001)
1.746 1.130 .494 −1.281 −.634 .183
.081 .258 .621 .2 .526 .855
(.002, 68.551)
−.408
.683
(1.096, 3.264)
2.290
.022*
(.485, 2.444) (.848, 3.772) (.771, 1.106) (.940, 1.031) (.997, 1.002) (.998, 1.003)
.206 1.527 −.867 −.684 −.348 .290
.837 .127 .386 .494 .728 .772
(.004, 39.040)
−.399
.69
(1.085, 5.655)
2.153
.031*
(1.555, 6.852) (4.799, 23.759) (.685, .985) (.921, 1.028) (.999, 1.006) (.995, 1.002)
3.126 5.804 −2.127 −.972 1.431 −.877
.002* < .001* .033 .331 .152 .38
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Table 2. Continued Variables
Odds ratio
Standard error
Salute Intercept .008 15.098 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 1.533 1.228 Nursing interventions (level 0 as reference) Level 1, 2 5.229 1.277 Level 3, 4, 5 3.945 1.313 GA 1.031 1.097 Age .983 1.024 BBW 1.000 1.001 BW 1.000 1.001 Sneezing Intercept .013 2850.629 Energy expenditure (120 < HR < 140 and 32.21 < ee < 37.21 as reference) HR < 120, ee > 37.76 or HR > 140, ee > 37.21 8.457 2.034 Nursing interventions (level 0 as reference) Level 1∼5 .460 2.126 GA .846 1.431 Age .950 1.033 BBW .998 1.002 BW 1.003 1.003
95% confidence interval
Z
(.000,1.706)
−1.763
p value .078
(1.025, 2.292)
2.081
.037*
(3.237, 8.445) (2.313, 6.730) (.861, 1.236) (.938,1.031) (.998, 1.002) (.998, 1.002)
6.762 5.037 .335 −.709 .354 −.109
< .001* < .001* .737 .478 .723 .913
(.000, 75,917.73)
−.547
.584
(2.104, 33.996)
3.008
.003*
−1.029 −.466 −1.563 −.958 1.185
.304 .641 .118 .338 .236
(.105, 2.019) (.419, 1.709) (.891, 1.013) (.995, 1.002) (.998, 1.009)
Note: BBW, birth body weight; BW, body weight; CI, confidence interval; ee, energy expenditure; GA, gestational age; HR, heart rate. *p < .05.
Energy expenditure was positively and significantly associated with grimace (p < .001, adjusted odds ratio: 2.262, 95% confidence interval [CI]: 1.558–3.284), sucking (p = .001, adjusted odds ratio: 2.397, 95% CI: 1.444–3.979), diffusion squirm (p = .003, adjusted odds ratio: 1.567, 95% CI: 1.163– 2.112), fist (p = .022, adjusted odds ratio: 1.892, 95% CI: 1.096–3.264), gape face (p = .031, adjusted odds ratio: 2.477, 95% CI: 1.085–5.655), salute (p = .037, adjusted odds ratio: 1.533, 95% CI: 1.025–2.292), and sneezing (p = .003, adjusted odds ratio: 8.457, 95% CI: 2.104–33.996). After adjustment for the effects of time, GA, birth days, birth body weight, and body weight, there were significantly increasing relationships between different levels of nursing interventions (levels 1–5) and these seven specific behaviors (Table 2). In other words, the odds ratios of these different specific behaviors being present increased with respect to the increase of levels of nursing interventions. DISCUSSION
Grimace is the most common stress behavioral response of infants toward painful stimulations and any other interventions (Mitchell, Brooks, & Roane, 2000). After multivariate adjustment, factors signifiJournal for Specialists in Pediatric Nursing 19 (2014) 331–338 © 2014, Wiley Periodicals, Inc.
cantly associated with grimace were energy expenditure and different levels of nursing intervention. The odds of exhibiting grimace were 2.262 times higher for infants with higher levels of energy expenditure compared with those with lower levels of energy expenditure (Table 2). Based on these results, neonatal caregivers should carefully observe preterm infants’ facial expressions while applying interventions in order to maintain the energy reserves of these infants. In this research, sucking is also positively related to energy expenditure and receiving different nursing interventions (p = .001). Infants with higher levels of energy expenditure were more likely to show sucking than those with lower levels of energy expenditure while receiving different interventions. However, a previous study (Ernst et al., 1989) demonstrated no effect on energy expenditure. Pinelli and Symington (2005) also made the same statement based on their literature reviews and meta-analysis. Sucking on a pacifier, nonnutritive sucking, during gavage feeding may improve the digestion of feeding and may also have a calming effect on infants; this is a common self-regulatory behavior of preterm infants suffering environmental stress (Als, 2007; VandenBerg, Browne, Perez, & Newstetter, 2003). Because this study’s method of measuring energy 335
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expenditure differed from that of other studies, further research might be needed into this issue. This research also found significantly positive relationships between energy expenditure and five stress behaviors (diffusion squirm, fist, gape face, salute, and sneezing) in preterm infants. After multivariate adjustment, diffusion squirm was significantly related to energy expenditure (p = .03). The odds of exhibiting diffusion squirm were 1.567 times higher for infants with higher levels of energy expenditure than for those with lower levels of energy expenditure. Similarly, after multivariate adjustment, fist was significantly related to energy expenditure (p = .022). The odds of exhibiting fist were 1.892 times higher for infants with higher levels of energy expenditure than for those with lower levels. After multivariate adjustment, there was a significantly positive relationship between sneezing and increased energy expenditure (p = .03). Infants with higher levels of energy expenditure were more likely to have sneezing than those with lower levels (adjusted odds ratio = 8.457, 95% CI = 2.104–33.996). After multivariate adjustment, factors significantly associated with gape face were energy expenditure and different levels of interventions (p = .031). The odds of exhibiting gape face were 2.477 times higher for infants with higher levels of energy expenditure compared with those with lower levels. Energy expenditure and various interventions were significantly correlated with salute (p = .037). The odds of exhibiting salute were 1.533 times higher for infants with higher levels of energy expenditure compared with those with lower levels. This current study is the first investigation to closely explore the relationships between behavioral stress responses and energy expenditure in preterm infants while they received nursing interventions. Our research findings indicate that preterm infants expend more energy when they show sucking, grimaces, or any of five stress behaviors (diffusion squirm, fist, gape face, salute, and sneezing) while receiving nursing interventions. Several studies have also found an assumption that reducing the need for stress or self-regulatory behaviors in preterm infants may conserve energy for their growth (Hulzebos & Sauer, 2007; Grenier et al., 2003; Guilfoy et al., 2008). Our findings help to verify this assumption. Neonatal clinicians should assess preterm infants’ energy levels and their stress behavioral responses while conducting nursing interventions. 336
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LIMITATIONS
Research methods used in this study may influence the generalizability of the results. The measurement of research data in the original study was recorded every 2 min, which may overlook some important factors affecting stress behaviors and the measurements of energy expenditure. Moreover, the small sample size could produce a significant bias. Most participants were born near 32 weeks GA, which may limit generalizability. Further research should investigate a larger sample size and include infants of different GAs.
How might this information affect nursing practice?
Research findings demonstrated significantly positive correlations between specific behaviors and levels of energy expenditure in preterm infants. Research findings also illuminated the possibility of continuous monitoring of the energy expenditure of preterm infants, which is important for neonatal caregivers wishing to provide quality interventions to their patients. Because of their immature physiological mechanisms, preterm infants are easily overtaxed and show exhausted states while experiencing environmental overstimulation (Als, 2007). Many fragile preterm infants at this critical physiological time are obtunded and show few stress behavioral responses because of low energy levels (Walden, Sudia-Robinson, & Carner, 2001). Although determination of valid measures of stress behavioral cues in preterm infants during nursing interventions is necessary, the amount of their energy expenditure that is available for response should be considered. In order to provide the protective, nurturing interventions that will help preterm infants conserve energy and achieve physiological stability, there is a need for neonatal nurses to understand the energy expenditure of their patients. Based on our research, we strongly suggest that caregiving during this critical medical time should be flexible according to the infant’s physiological needs, indicated by their stress behaviors and conditions of energy expenditure.
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