The care of neonates who are born prematurely has focused on improving mortality and morbidity since the development of the first hospital-based premature nursery at Michael Reese Hospital in Chicago in 1922. 1 Moreover, with advanced neonatal intensive care, interventions improved survival of neonates born at <37 weeks of gestation has continued over the past years 2–8 thus increasing the number of preterm survivors from 9.4% in 1980 to 11.5% in the year 2000. 9 On the basis of the most recent National Vital Statistics Report, for the year 2000, 11.5% of the 4,058,814 live births in the United States were premature (<37 weeks gestation). 9 Nearly 10% of the total live births occurred between 30 and 35 weeks gestation and >50% of the total live preterm births occurred between 30 and 35 weeks gestation. 9 The latter group is the largest cohort of reported live preterm births in the United States. With improvement and stabilization of the mortality rate of all preterm births, investigations have focused on the ensuing morbidities associated with preterm birth. Conversely, there has been a shift toward investigating the outcome for babies of both low birth weight (LBW) born preterm 10–23 and extremely low birth weight (ELBW) born very preterm, 24–33 although babies in this latter category account for only a small fraction (approximately 1%) of the total live births. 9
Regardless of which preterm cohort is the focus of research, multiple problems have been noted in the developmental follow-up literature to preclude drawing firm conclusions about the outcome of children born preterm, despite the fact that follow-up of preterm infants is well documented. 2–8,10–34 The problems identified in a meta-analysis 34 of literature on follow-up of infants born preterm included inadequate description of subject population, little or no consideration of perinatal course, lack of appropriate comparison groups, no assessment of the child’s home environment or family demographics, global or vague outcome measures, and lack of homogeneity of the subjects, eg, a mixed sample of children born preterm with and without frank impairments, and mixed sample of children born preterm and categorized as small for gestational age and appropriate for gestational age.
An additional problem with these follow-up studies has been the emphasis on assessment of major and minor morbidities early in the life of the child, rather than at school age and beyond when the effect of preterm birth may affect functioning in school or health. For example, only six studies 35–40 investigated cardiorespiratory endurance in school-age children with history of preterm birth and many of the studies featured the problems identified in a meta-analysis conducted by Aylward et al. 34 Furthermore, no studies have investigated health-related fitness or physical activity levels of school-age children born preterm.
Health-related fitness includes the components of cardiorespiratory endurance, muscular strength and endurance, flexibility and body composition, and is characterized by the ability to perform daily activities with vigor and a low-risk of premature development of disease attributed to inactivity. 41 Physical therapists who are working with children born preterm should be concerned with health-related fitness as it relates to day-to-day activity limitations or participation restrictions for the purposes of health promotion and disease prevention. The Guide to Physical Therapist Practice42 states that physical therapists in the context of patient/client management may identify disablement risk factors and buffer the disablement process by promoting health, wellness, and fitness. Practice Pattern 6A is devoted to primary prevention/risk reduction for cardiovascular/pulmonary disorders. By itself, physical inactivity is a risk factor for many diseases and conditions thus affecting morbidity and life expectancy. Data support an inverse association between physical activity and premature mortality in adults. 43,44 Physical activity and fitness is a focus area of Healthy People 201045 in which objectives stress the importance of moderate and vigorous physical activity for children, with the hope that physical activity patterns adopted early in life continue into adulthood. It is important to identify inactivity risks and examine early childhood conditions in the context of later health and fitness status. No previous studies have examined health-related fitness or activity levels of children with history of preterm birth. Therefore, the purpose of this study was to investigate health-related fitness and physical activity levels of children seven to 10 years of age born five to 10 weeks preterm.
This study was a cross-sectional case control prospective design of 44 subjects between the ages of seven and 10 years. Twenty-two children born preterm were recruited into the preterm group and 22 children born full term matched by gender, age and race were recruited into the control group. This sample size was based on a power analysis computation of 0.8 and a medium effect based on Cohen’s tables. 46 The children in the preterm group had a history of preterm birth between 30 and 35 weeks gestation, were appropriate for gestational age (AGA) and exhibited no congenital anomalies. The subjects in the preterm group were recruited primarily from a letter mailed by the chief neonatologist to parents of neonatal intensive care unit graduates informing them of the study and inviting them to contact the study coordinator. Subjects in the preterm and control group were also recruited from the region by advertising in local newspapers, churches, schools, and recreation centers and by referral from other subjects.
Children in the preterm group were excluded from the sample if they had cardiac disease, joint disease, asthma, bronchopulmonary dysplasia, periventricular leukomalacia, cerebral palsy, mental retardation or other major neurological disability. Control group subjects were excluded from the sample if they were born at <38 weeks gestation, had a birth weight below the 10th percentile, a history of neonatal complications, demonstrated school-related difficulties, had received any special education, or were currently being treated for or had a history of musculoskeletal, cardiac, or pulmonary disease. Contraindications to participating in the testing for children in either the preterm and control group included the following: acute cardiac, pulmonary, or renal inflammation, elevated body temperature, and blood pressure >140/90 mm Hg. The author obtained Human Subjects approval before data collection. Table 1 outlines the tests and measures used in this study.
Anthropometric measurements included body weight in kilograms and height in centimeters, using a beam balance scale and stadiometer (Cardinal Detecto Physicians Scale, Cardinal Scale Co., Webb City, Mo), respectively, and mean skinfold thickness in millimeters at three sites. Skinfold thickness of the area over the triceps, subscapular area and medial calf was measured using skinfold (Lange, Beta Technology, Inc., Santa Cruz, Calif) calipers on the right side of the body. Three readings were taken at each site if there was not a 90% agreement between the first two readings. Measurements were recorded to the nearest 0.5 mm. The percentage of body fat was calculated using mean skinfold thickness at all three sites using the body fat equations of Slaughter et al. 47
Flexibility was examined with the use of the sit-and-reach test; measures of elbow extension, knee extension, thumb to wrist, and fifth metacarpophalangeal extension using a goniometer; and palm to floor using a ruler. The sit-and-reach test was measured using a standardized sit-and-reach flexibility tester (Lafayette Instrument Co., Lafayette, Ind) by following manual instructions. The remaining flexibility tests and measures followed the protocol for assessing joint laxity established by Beighton et al. 48
Joint laxity was assessed at the following five sites with one point given for achievement of each of the following positions: 1) passive extension of the fifth finger beyond 90 degrees on the dominant side; 2) passive apposition of the thumb to the flexor aspects of the forearm on the dominant side; 3) hyperextension of the elbow beyond 10 degrees on the dominant side; 4) hyperextension of the knees in supine beyond 10 degrees; and 5) forward flexion of the trunk, with the knees straight, so that the palms of the hands rested easily on the floor. The maximum joint laxity score was five. To enhance internal reliability of these measures, one physical therapist was trained in the protocol-measured flexibility of all subjects. Reliability in testing and scoring was 0.95. Additionally, the physical therapist examiner measuring flexibility was blind to whether the subject was in the preterm or control group to prevent observation bias.
Muscular Strength and Endurance
Muscular strength and endurance for each subject was examined using the Bruininks-Oseretsky Test of Motor Proficiency (BOTMP). 49 The BOTMP, a gross motor test and measure, is a standardized norm-referenced tool used for children between 4½ and 14½ years of age. Only the four gross motor subtests (running speed and agility, balance, bilateral coordination, and muscle strength) were administered. Administration and scoring procedures followed the standardized protocol as outlined in the BOTMP manual. 49 The reliability coefficient reported in the BOTMP manual for the gross motor composite was reported to be 0.77. 49 To enhance internal reliability one physical therapist examiner performed the BOTMP on all subjects. The examiner, a pediatric physical therapist with over 20 years of experience, was well acquainted with the tests and with examining children. Before the initiation of the study, the primary investigator reviewed the standardized administration and scoring procedures with the physical therapist examiner. Before data collection, the physical therapist examiner administered the tests to children who were not in the sample. Additionally, to prevent observation bias the physical therapist examiner was blind to whether the subject was in the preterm or control group.
To determine the difference in cardiorespiratory response to exercise between the groups, the subjects performed a maximal treadmill exercise test on a MedGraphics Trackmaster (model 225, Medical Graphics Corp., St. Paul, Minn) using the Bruce treadmill protocol. 50 The subjects exercised in shorts and running shoes in an air-conditioned laboratory. Each child was introduced to the exercise test and Borg Rate of Perceived Exertion (RPE) scale 51 with a standardized script prepared by the primary investigator. Each child wore a nose clip so that all inspired and expired gases were routed through the mouthpiece. Gas exchange parameters were measured breath-by-breath using a metabolic cart (MedGraphics CPX/D, Medical Graphics Corp.) and software (BreezeEX; Medical Graphics Corp.). The system was calibrated before each session with standard gases of known oxygen and carbon dioxide parameters. A heart monitor (Polar Electro Inc., Woodbury, NY) was worn by each child along with a specially adapted transducer (Medical Graphics Corp.) to record heartbeat with software analysis.
After pre-exercise heart rate (HR) and oxygen consumption (VO2) were recorded, the subjects participated in a continuous graded protocol involving stages at which the speed and grade progressively increased at three-minute intervals from 1.7 to 6 MPH and from 0 to 22 degrees, respectively. The Bruce protocol, very suitable for children, 50 begins very slowly at 0-degree grade and gradually increases speed and grade, thereby easing the child into the demands of the test. The subjects were verbally encouraged to exercise to the limit of their tolerance. Rate of perceived exertion was recorded at the end of each three-minute stage. Heart rate was monitored prior to exercise, continuously during exercise, and for two minutes after completion of the maximal exercise test. Blood pressure was monitored before exercise and two minutes following completion of the maximal exercise test. Metabolic gas measurements were analyzed, recorded and saved. Ventilation and gas exchange was measured breath-by-breath immediately before, during, and three minutes after exercise. VO2 and respiratory exchange ratio (RER) were monitored and recorded every two minutes. The treadmill test was terminated when the subject exhibited signs of excessive fatigue or dyspnea, complained of pain, headache, or dizziness precipitated by the exercise, became unsteady on the treadmill, or communicated the need to stop. During the recovery phase, the subjects walked at a rate of 2.2 MPH at a 0-degree grade for four minutes.
Physical Activity Questionnaire
Before the appointment or on the day of the testing appointment, both the child and parent completed a questionnaire that had previously been piloted and validated. 52,53 The questionnaires gathered information on the child’s level of previous habitual physical activity and engagement in sports based on the parent’s and child’s perspective.
Before the appointment or at the testing appointment, the parents completed a demographic questionnaire created by this investigator. The number of family members, maternal and paternal level of education and years of education, as well as family income were variables included in this questionnaire.
With written consent from the parent, birth records of the children born preterm were obtained. Variables associated with preterm delivery, such as intubation, ventilation, and length and use of supplemental oxygen, number of doses of exogenous surfactant, and results from cranial sonogram were examined as predictor variables.
Data were managed and analyzed with the use of a Statistical Package for the Social Sciences (version 10.1, SPSS, Chicago, Ill). Descriptive statistics were calculated for both groups on the following physical characteristics: gender, age, birthweight, gestational age, height, weight, body mass index (BMI), mean measurement of skin folds, percent body fat, and the results of the physical activity and demographic questionnaires. Paired t tests (α = 0.05) were calculated on the dependent variables in each component of health-related fitness and physical activity. Nonparametric tests were performed on nominal and ordinal data.
This study was a cross-sectional case control prospective design of 44 subjects between the ages of seven and 10 years. Twenty-two children born preterm were recruited into the experimental group and 22 gender, age, and race-matched children born full term were recruited into the control group. Because of the homogenous population from which the sample was recruited, the final sample consisted of 22 white females and 22 white males. Subject characteristics are reflected in Table 2.
Analysis of the responses on the demographic questionnaire revealed no significant difference between the preterm and control group in family income (z = 0.427, Mann-Whitney U test). All parents had completed a high school education. The family unit of the control group was statistically significantly larger (p = 0.027).
The previously piloted physical activity questionnaires 52,53 were completed by the child and parent. Paired t tests revealed no significant differences between the groups (Table 3). Although the control group reported exercising one day per week more, this did not reach statistical significance. The reported range for exercising, strengthening, stretching, and walking was the same for both groups. The subjects in both the preterm and control group reported involvement in either school or extracurricular sports in the past 12 months (Table 4). The majority of parents of both the preterm and control group stated that their child was as active as their friends, had no complaint during or after exertion and was as active as they should be (Table 5). More parents of children born preterm reported that their child often had bruises. Parent report corroborated their child’s report of involvement on sports teams.
Each child in the preterm group was matched within 10% BMI to a control group subject. Even with the 10% BMI match, significant differences in weight and height were found between the preterm and control group. When the weight and height for each subject were plotted on the National Center for Health Statistics 54 height/weight chart, all preterm subjects were over the 10th percentile, except one subject, who was below 5% for both height and weight. All control subjects were at or over the 25th percentile. Therefore, all but one preterm and all control group subjects were within normal values for height and weight. No differences were found between the preterm and control group in the mean skinfold value for the three measured sites or percentage of body fat based on prediction equations by Slaughter et al 47 (Table 6).
Flexibility was examined using the sit-and-reach test and at five sites following the joint laxity protocol by Beighton et al, 48 ie, elbow extension, knee extension, thumb to wrist, palm to floor, and fifth metacarpophalangeal extension. The results of the sit-and-reach test were recorded in centimeters. The joint laxity test was measured on a scale of 0 to 5 based on the subject’s ability to perform the actions. A paired t test (Table 7) examining differences on the sit-and-reach revealed no significant differences between groups. Wilcoxon signed-ranks test was completed on the joint laxity results to examine the differences, direction of the difference and relative amount of difference between groups. It was hypothesized that there would be differences in flexibility, with the preterm group exhibiting greater flexibility. However, a statistical difference in flexibility was not found between the groups on the sit-and-reach test or the joint laxity test. Although the control group subjects were able to reach a greater distance than the preterm group on the sit-and-reach test, this was not statistically different. On the joint laxity index, four preterm subjects had less joint laxity than the paired control group; eight preterm subjects had equal joint laxity to the paired control group and 10 preterm subjects had greater joint laxity than the paired control group.
Muscular Strength and Endurance
It was hypothesized that the preterm children would demonstrate a significant difference in muscular strength and endurance as measured on the BOTMP, Gross Motor Composite (running speed and ability, balance, bilateral motor coordination and strength). Correcting for multiple t tests, α = 0.0125 after a Bonferroni correction (0.05/4), a significant difference was found in the gross motor composite between the preterm and control groups. Further examination of the subtests revealed a statistical difference (α = 0.0125) in running speed and agility, balance, and strength (Table 8).
The norm-referenced test mean of the BOTMP gross motor composite is 50 with a standard deviation (SD) of 10. Further analysis of the BOTMP results, as illustrated in Figure 1, revealed that only one control group subject had a standard score ≤ 40 (−1 SD below the norm-referenced mean) and one control group subject had a standard score ≤ 30 (−2 SD below the norm-referenced mean). All other control group subjects were above −1 SD with four control group standard scores greater than or equal to +3 SD above the norm-referenced mean. In contrast, 10 preterm subject standard scores were ≤ −2 SD.
It was hypothesized that the children in the preterm group would demonstrate a significantly different response to cardiorespiratory endurance exercise as measured on a maximal treadmill test. A statistical difference in cardiorespiratory response to exercise between the preterm and control group in terms of VO2peak, heart rate at VO2peak, RER, or total exercise time was not demonstrated. (Table 9) However, the control group tolerated the maximal exercise longer and achieved a RER of >1.0. The RER is a ventilatory measurement that reflects gas exchange between the lungs and the pulmonary blood. The RER exceeds 1.0 during maximal exercise due to hyperventilation and buffering of lactic acid in the blood. An RER of 1.15 or more is indicative of maximal effort in an adult 55 and 1.0 or more indicates a maximal effort in a child. 56 The mean RER of the control group was 1.01, indicating a maximal effort, whereas the preterm group mean RER was 0.95.
The hospital neonatal intensive care admitting report and discharge summary were obtained with parental consent from all but one subject whose records could not be located. Therefore, neonatal records from 21 subjects born preterm were examined. The following variables were examined: age at discharge, respiratory diagnosis, oxygen use, and method of O2 delivery, age weaned to room air, administration of surfactant, and results from cranial ultrasound. Fifteen of the 22 subjects born preterm had a diagnosis of respiratory distress syndrome. Four subjects did not meet the criteria for respiratory distress syndrome, while one summary made no reference to the neonate’s respiratory status. Two subjects had evidence of Grade I intraventricular hemorrhage (IVH) on the cranial sonogram. Six summaries did not mention anything about a cranial sonogram procedure. Twelve subjects had cranial sonograms that were documented as within normal limits. Five subjects had one surfactant dose administered at birth and one subject had three surfactant doses administered at birth. Descriptive statistics on age at discharge and age weaned to room air are illustrated in Table 10.
Post Hoc Calculation of Effect Size
A way of measuring the degree of departure from the null hypotheses is to calculate effect size. According to Cohen, 46 effect size is the measure of magnitude of the differences between sample means or an estimate of the effect of the independent variable (preterm birth) on the dependent variables (health-related fitness). The effect size associated with a t test is d, defined as d = (mean of control group minus mean of experimental group)/mean standard deviation. According to Cohen’s conventions, 0.2 is a small effect, 0.5 is a medium effect, and 0.8 is a large effect. The effect-size estimate was calculated on all dependent variables of the health-related fitness components. Those dependent variables that had an effect size of 0.5 or more are illustrated in Table 11, with the p value from the paired t test. The variables weight, height, muscular strength and endurance, total exercise time on treadmill, and RER had medium-to-large effect sizes.
This study investigated the health-related fitness and physical activity levels of children aged seven to 10 years who were born five to 10 weeks preterm. More specifically, the subjects in the preterm group were AGA, pre-pubescent, Caucasian, and similar in demographics to the control group. Control group subjects were matched based on gender, age, and race and were within 10% on body mass index. Efforts were made a priori to alleviate the weaknesses in previous preterm literature as identified by the Aylward et al 34 meta-analysis, such as inadequate description of subject sample, little or no consideration of perinatal course, lack of appropriate comparison groups, no assessment of the child’s environment or demographics, global or vague outcome measures, and lack of homogeneity of the subjects, eg, mixing sample of children with and without frank impairments and mixing sample of children categorized as SGA and AGA. Additionally, the cohort selected for study represented the greatest percentage of reported preterm births. 9 Moreover, no published studies have examined the implications of preterm birth on health-related fitness and physical activity at school age.
A number of conclusions can be drawn from this study. Despite the match between paired subjects’ BMI to 10% or less, significant differences were found in height and weight. Many authors investigating outcomes of preterm birth at school age have reported no differences in height and weight 20,35,38–40 between the preterm cohort and term controls. However, several other authors have reported a difference in height 57–59 or weight 28,60 or both. 61,62 Physical growth and body size, although strongly influenced by genetics, may provide an index of early environmental effects of a developing organism and is worthy of continued study with the preterm cohort. In addition, the fact that no difference in body fat was found between the groups but a significant difference in weight was found, may imply that the child born preterm has less muscle mass available to contribute to muscular strength and endurance measures.
Gestational age is determined, in part, by joint laxity and the lack of firmness of collagen in the neonate. According to the Dubowitz Scale, 63 the more preterm the neonate is, the greater the collagen extensibility and joint laxity. Moreover, preterm neonates exhibit hypotonicity 64 that often extends until school age. 22 Hypotonia is frequently associated with joint hyperextensiblity. 64 This study revealed no significant differences between the preterm and control group subjects in joint flexibility as previously hypothesized. However, no previous studies have been published that investigate flexibility of school age children with history of preterm birth.
Motor skill impairments at school age have been reported in previous studies of children born preterm with similar gestational age and birth weight characteristics as the subjects in this study. 19–21,65,66 However, these studies relied on anecdotal observations, 66 used criterion referenced motor tests to quantify motor skills 21 or used tests that examined the degree of impairment and not skill ability. 19,20,65 In contrast, this study utilized a norm-referenced standardized gross motor test. The results demonstrated that only six subjects in the preterm group were able to perform gross motor skills at or better than the BOTMP norm-referenced mean of 50, in contrast to 19 full-term controls. Therefore, 16 children in the preterm group scored at or below −1 SD below the mean. Children with scores falling at least 1 SD below the mean are considered to have clinically inferior motor performance. 67 Moreover, on the basis of the parent report, only four subjects in the preterm group were referred for early intervention services following discharge from the neonatal intensive care nursery. Based on the results from the physical activity questionnaires no significant differences were found in the level of reported physical activity or involvement in extracurricular sports. Fortunately, the demonstration of impairments in muscular strength and endurance in the preterm group did not contribute to physical activity limitations 68 (difficulties an individual may have in executing activities), or participation restrictions 68 (problems an individual may experience in involvement in life situations).
Despite the evidence of impairments in muscular strength and endurance between the preterm and control group, performance on the maximal treadmill test yielded no statistical differences in VO2peak, HR max, total time on the treadmill or RER. However, attaining maximal effort on treadmill testing is challenging for children due to the lack of motivation. 56 For example, neither group achieved a predicted heart rate maximum based on the convention of 220–age 55 (>210 for this age cohort). The maximal effort of the control group was greater than the preterm group when expressed as achievement of an RER of >1.0, an indication of maximal effort. 56 Examining the results from the studies that have investigated cardiorespiratory endurance in children born preterm, only Gross et al 36 and Jacob et al 38 found no difference in VO2peak. Baraldi et al 35 did not report the results from the control group, only providing results for those who were AGA and SGA. Heldt et al 37 did not employ a control group. Santuz et al 40 found subjects in the preterm group had a significantly lower VO2peak although everyone in the preterm group had a diagnosis of bronchopulmonary dysplasia (BPD). Pianosi and Fisk 39 found that the VO2peak was statistically less in eight-year-old children with a history of preterm birth (AGA and without BPD) when compared to age, gender, and race-matched peers. More research is warranted in this area, especially with an older age group, where a full effort in the treadmill testing may be achievable.
Pediatric physical therapists frequently provide services to children born preterm. Consequently, it is important for therapists to be knowledgeable about the health-related outcomes of preterm birth. Primary prevention and risk reduction for cardiovascular and pulmonary disorders is an important role of physical therapists so that the client may 1) achieve optional functional capacity; 2) minimize impairments, functional limitations and disabilities related to congenital and acquired conditions; 3) maintain health; and 4) enhance independent function. 42 In addition, physical therapists providing early intervention services to children born five to 10 weeks preterm have opportunities to inform parents of the probable health-related outcomes for their child at school age.
This study demonstrated that school-age children born five to 10 weeks preterm exhibited impairments in muscular strength and endurance. However, these impairments did not impact cardiorespiratory endurance on a maximal treadmill test or reported involvement in physical activity or sports. Children born five to 10 weeks preterm, who are AGA with minor perinatal risks (ie, no respiratory sequelae such as BPD and no IVH or only a Grade I IVH), exhibit minor differences in health-related fitness when compared to matched controls that are born full term. The findings of this study imply that children at school age with history of preterm birth will be as active as their peers. At school age, they are able to perform daily activities with vigor constituting a low-risk for premature development of disease attributed to inactivity.
Despite the minor differences in health-related fitness, it would be beneficial to examine physical self-concept between the groups. The Piers-Harris Children’s Self-Concept Scale 69 has eight items that measure self-perception of physical attributes, eg, the perception of being strong, clumsy, or a leader in games and sports. School-age children with history of preterm birth who exhibit motor impairments may perceive themselves as clumsy or being among the last to be chosen for games, therefore affecting self-esteem.
Reproducing this study with adolescents with a history of preterm birth is warranted, when a full effort on cardiorespiratory testing may be attained, when competitive extracurricular sports are initiated and when, in general, physical activity is noted to decline. 70 Furthermore, future investigations may determine whether the deficiencies in muscular strength and endurance noted in the school-age child born five to 10 weeks preterm affects future self-esteem, physical adeptness, and involvement in sports activities in adolescence.
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