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First published online October 26, 2006
British Journal of Radiology (2007) 80, 401-405
© 2007 British Institute of Radiology
doi: 10.1259/bjr/55460700
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Full paper

Phalangeal quantitative ultrasound measurements in former pre-term children aged 9–11 years

Z P Halaba, MD 1 J Bursa, MD, PhD 2 U Kostowska Kaplon, MD 2 W Pluskiewicz, MD, PhD 3 S Marciniak, MD 4 and U Drzewiecka, MD 5

1 Public Clinical Hospital No 1 in Zabrze, Poland, 2 Pediatric Intensive Care Unit in Zabrze, Department and Clinic of Pediatrics, Silesian School of Medicine in Zabrze, Poland, 3 Metabolic Bone Diseases Unit, Department and Clinic of Internal Diseases, Diabetology and Nephrology, Silesian School of Medicine in Zabrze, Poland, 4 Regional Hospital in Zabrze, Poland, 5 Regional Hospital in Kraków, Poland

Correspondence: Zenon P Halaba, Public Clinical Hospital No 1 in Zabrze, 3-go Maja Street 13/15, 41-800 Zabrze, Poland. E-mail: zhalaba{at}poczta.onet.pl


   Abstract
Top
 Abstract
Introduction
 Methods and subjects
 Results
 Discussion
 References
 
The objective of this study was to compare phalangeal ultrasound values in 38 former pre-term children, aged 9–11 years, with 50 age-matched term controls. Skeletal status was evaluated using phalangeal quantitative ultrasound measurements (QUS) by DBM Sonic 1200 (IGEA, Carpi, Italy) which measures the amplitude dependent speed of sound (Ad-SoS, m s–1). There were no significant differences in values of Ad-SoS, weight and height between patients and controls irrespective of birth weight or prematurity. In conclusion, phalangeal ultrasound measurements performed in prematurely born infants show that at the age of 9–11 years their bone status does not differ from children born at term.


   Introduction
Top
 Abstract
 Introduction
Methods and subjects
 Results
 Discussion
 References
 
Metabolic bone disease (MBD) of prematurity is common and inversely related to birth weight and gestational age [1, 2]. Some diseases such as bronchopulmonary dysplasia, chronic treatment with loop diuretics and corticosteroids as well as prolonged immobilization may influence bone metabolism. Some studies have shown that bone mineral density [3–6] and ultrasound values [7] are reduced in premature infants, particularly those with very low birth weight (VLBW) compared with full-term infants. The risk of osteoporosis might also be modified by environmental influences during early life. In accordance with the theory of programming [8], persisting changes in the structure and function caused by environmental factors during critical periods of early development may be translated into pathology and determine disease in later life. Lack of nutrients and oxygen during prematurity are the strongest factors acting at this critical period. The long-term effects of low birth weight and prematurity on bone still need explanations. In recent years, the method of quantitative ultrasound (QUS) for assessing bone properties has been developed. QUS techniques hold great potential for the assessment of bone structure and the possibility of predicting fracture risk in children. Low-frequency ultrasound travels across bone with a velocity that is related to bone quality and density. Therefore, it seems QUS techniques may be less influenced by bone size [9]. Furthermore, QUS can reveal physical properties of bone determined by bone composition and by structure [10]. QUS is also void of ionizing radiation, cost effective, easy to use and portable so its features are beneficial in paediatrics. QUS systems exist for measurements at various skeletal sites such as calcaneus, phalanges, tibia and patella. Several recent studies suggest that phalanges may be an appropriate measurement site because this site is sensitive to changes in bone status [11–15]. Skeletal development begins in utero and continues at least through the first two decades. The amount of skeletal mass acquired during this period is one of the most important determinants for the risk of osteoporosis. Childhood and adolescence are crucial periods for the formation of a skeleton [16, 17]. Many factors have an influence on peak bone mass. The main determinants of peak bone mass are genetic factors, hormonal status, calcium intake and physical activity [18–20]. The ability to modify some of these factors may positively influence bone mass and prevent osteoporosis in the elderly. Since early prevention of osteoporosis is likely to be more successful than treatment of the established disorder this requires a better knowledge of bone mass acquisition and identification of individuals at risk. The aim of the present study was to compare phalangeal ultrasound values in former pre-term children, aged 9–11 years, with age-matched term controls and examine the possibility that prematurity or low birth weight might be a risk factor for the later development of osteoporosis.


   Methods and subjects
Top
 Abstract
 Introduction
 Methods and subjects
Results
 Discussion
 References
 
The study population comprised 38 children aged 9–11 years (25 boys and 13 girls). All have been admitted to the Paediatric Intensive Care Unit in Zabrze at the Silesian Medical School (Katowice, Poland) during their neonatal period (1993–95) due to disturbances of post-natal extrauterine adaptation resulting from prematurity and respiratory failure. The Apgar score ranged from 0 to 10 (median 5) at the first minute of life and from 1 to 8 (median 6) at the fifth minute. The mean gestational age was 34 weeks±3 weeks, mean birth weight was 2126 g±543 g and mean body length at birth was 48 cm±5.7 cm. 36 of the pre-term newborns were appropriate for gestational age (AGA), one was small for gestational age (SGA) and one was large for gestational age (LGA). During their stay in the Paediatric Intensive Care Unit, 29 newborns were treated using mechanical ventilation (including nine nasal continuous positive airway pressure (nCPAP)). The time of ventilation ranged from 2 days to 54 days (mean 10 days) and the time of hospitalization ranged from 15 days to 137 days (mean 43 days). Children had medication known to affect bone metabolism (i.e. corticosteroids, anticonvulsant etc.). The control group consisted of 50 term born children (GA> 37 weeks), Apgar score 7–10 (median 8). It included 33 boys and 17 girls with birth weight higher than 2500 g. All children were enrolled in the study after informed parental consent was obtained. The study protocol was approved by the Committee of Ethics and Supervision of Research on Humans and Animals at the Faculty of Medicine of the Silesian Medical School in Katowice.

In all subjects ultrasound measurements were performed with a DBM Sonic 1200 device (IGEA, Carpi, Italy). The device is equipped with two probes mounted on an electronic calliper. The emitter probe positioned on the medial surface of the measured phalanx generates a single period at least 1.25 MHz every 128 µs. The receiver probe is positioned on the lateral side of the phalanx and obtains the ultrasound that crossed the phalanx. The time interval between emission and reception of the ultrasound signal is measured and expressed in m s–1. Speed of sound in bone tissue was calculated considering the first signal with an amplitude of at least 2 mV at the receiving probe; thus, the measured speed of sound is amplitude dependent (Ad-SoS). The phalangeal ultrasound system measures Ad-SoS at the distal metaphysis of the proximal phalanges of II–V fingers on each hand. There is no significant difference between measurements of both hands [11, 21, 22]. The final result is the average SoS over four fingers. Acoustic coupling is achieved using a standard ultrasound contact gel. Measurements were performed on the dominant hand by the same operator. In vivo short-term precision was assessed based on mean coefficient of variation for 75 measurements made in 15 healthy persons (eight boys and seven girls measured five times each). All these measurements were taken by the same operator with repositioning of the calliper. Coefficient of variance (CV%) was 0.64%. CV% was calculated according to the following formula: CV% = (SD/mean) x 100.

During puberty, gender-related differences in bone status are revealed. In our previous studies we reported no significant difference in Ad-SoS values between boys and girls up to the age of 11 years [15, 23]. The significant difference appeared in the age group of 12–15 years. Therefore results obtained for both boys and girls were analysed together.

Final data management and analyses were performed using the Statistica program for the IBM PC computer. The normality of data distribution was established using the Shapiro–Wilk test. Descriptive statistics (mean ± SD) were summarized for all variables. The significance of the differences between both groups was determined using Student's t-test and Mann–Whitney's test. The relationships between Ad-SoS values and age, body size and body birth parameters were assessed using simple linear regression analysis. p-value < 0.05 was considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Methods and subjects
 Results
Discussion
 References
 
There were no statistically significant differences in weight, height and the Ad-SoS values between our patients and the control group. The subjects' characteristics are given in Table 1Go. To assess the influence of birth weight on abnormal Ad-SoS the study group was subdivided into two groups with a birth weight of 2000 g or less and more than 2000 g. There were no statistically significant differences in weight, height and the Ad-SoS values between each subgroup and the control group and among them (Table 2Go). In the whole studied group, in the subgroups and controls, no significant correlations were found between Ad-SoS, weight and height, pubertal status or Apgar score staging at first and fifth minute and Ad-SoS did not correlate with gestational age and birth weight. We did not find any correlations between Ad-SoS value and ventilation times or length of hospitalizations.


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  		Table 1. Characteristics of studied and control group

 

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  		Table 2. Characteristics of studied population divided into two subgroups with birth weight less or more than 2000 g

 

   Discussion
Top
 Abstract
 Introduction
 Methods and subjects
 Results
 Discussion
References
 
Several studies have shown that pre-term infants could normalize their bone mineral density (BMD), especially in the lumbar spine during early childhood [3, 5, 24–28]. The majority of children studied were evaluated using dual energy X-ray absorptiometry (DXA), the method considered to be the gold standard in paediatrics. However, DXA had some essential limitations. DXA estimates only the level up to which a radiation beam is attenuated by a bone tissue that depends on a physical density, but on bone size as well. It means that a smaller bone may have a lower areal bone density than a larger bone [29]. It should be highlighted that DXA does not provide information about the quality of bone. Using phalangeal ultrasound we tried to assess features other than bone mass. QUS reflects bone properties that are independent of bone density measured by DXA [10]. Furthermore, QUS is influenced by dimensions of bone to a lesser extent than DXA [9]. At least for hand phalangeal QUS measurements using the DBM Sonic 1200 device there are several studies on normative values published from 1997 to 2004 [15, 22, 23, 30, 31]. The large children and adolescent populations from different European countries were measured and trends of changes in measured ultrasound parameters during childhood and puberty were comparable as shown in studies using DXA measurements [16, 17]. Furthermore, some studies were performed in young subjects with different diseases known to affect bone metabolism. In case–control studies QUS proved its utility in the detection of skeletal changes in subjects with genetic disorders [32], renal osteodystrophy [33, 34], acute lymphoblastic leukaemia [35] and in subjects treated with gonadotrophin-releasing hormone [36].

There are also some longitudinal studies in survivors of acute lymphoblastic leukaemia [37, 38] and in subjects with renal insufficiency [39].

Recently, phalangeal QUS and DXA measurements were compared in healthy subjects [40] and in patients with genetic disorders, which showed that QUS has the potential to express bone changes in comparison with DXA measurements. We chose 9–11-year-old children to obtain measurements just before the onset of puberty which has a major effect on skeletal mineralization but we acknowledge that the narrow age range is a weakness in the study. Helin et al [41] assessed the forearm bone mineral content (BMC) using photon absorptiometry in 75 children aged 4–16 years, who all had a low birth weight. They found that only boys who had been born pre-term had less BMC than the controls born at term, but they were also somewhat shorter and lighter. Similarly, Zamora et al [42] evaluated BMC and areal bone mineral density (aBMD) at various skeletal sites in former pre-term girls, aged 7–9 years. They reported that aBMD was lower in former pre-term compared with former term controls at the level of the radial metaphysis, femoral neck and total hip. Femoral neck aBMD remained lower when reassessed after 1 year. But there were no differences at sites with predominantly cortical bone. On the contrary Hori et al [24] measured lumbar spine bone mass in 21 pre-term children (gestational age 32±2 weeks and with birth weight of 1.764±0.467 g) aged 3–4 years by DXA and found that all of the 21 children had normal bone mineral content and density in comparison with the age-matched normal term children. The subgroup of children who were born more prematurely at GA < 32 weeks also had normal BMC and BMD. BMC and BMD showed a significant positive correlation with age and body weight. Similar outcomes were obtained by Ichiba et al [5] examining skeletal status by repeated DXA in Japanese VLBW infants (birth weight < 1500 g) aged 40 weeks post-conception to 3 years of age and in three control groups with birth weight 1500–1999 g, 2000–2499 g and more than 2500 g and showed that bone mass was normalized at 2 years of life in VLBW infants. Their height and weight were also normalized at this time. Similarly in our patients at the age of 9–11 years, i.e. at the pre-pubertal stage, Ad-SoS was not different in comparison with the control group. When our studied group was subdivided into two subgroups with a birth weight of 2000 g or less and more than 2000 g we did not find any statistically significant differences in weight, height and the Ad-SoS values between these subgroups and the control group. We hypothesize that quality of bone measured by Ad-SoS is similar to bone mass and is accomplished in the skeleton during childhood. The major changes in skeletal status occur during puberty. It is not certain if the gain in bone mass and quality of bone remains the same in premature infants and those born at term. This would require further study.

In our study group there were no significant correlations between QUS values and age and body weight. There was also no correlation between Ad-SoS values and Tanner stage but it was probably because the participants were only just at the onset of puberty. We did not find any correlations between Ad-SoS value and Apgar scores, ventilation times or length of hospitalizations. In contrast Bowden et al [43] using DXA found that the number of ventilator days was the factor most significantly correlating with a reduction in bone mineralization at the age of 8 years. The reason for this discrepancy is uncertain but might result from different techniques in assessing bone status or that their patients were born more prematurely or they were not the same weight at birth.

In conclusion, phalangeal ultrasound measurements performed in prematurely born infants show that at the age of 9–11 years their bone status does not differ from that of children born at term.

Received for publication February 20, 2006. Revision received August 22, 2006. Accepted for publication August 24, 2006.


   References
Top
 Abstract
 Introduction
 Methods and subjects
 Results
 Discussion
 References
 

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