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1 Department of Radiology and Imaging Center for Child Abuse and Neglect, UMass
Memorial Health Care, 55 Lake Ave. N., Worcester, MA 01655.
2 Present address: Department of Radiology, Hallmark Health—Melrose
Wakefield Campus, 585 Lebanon St., Melrose, MA 02176.
3 Present address: Department of Radiology, Johns Hopkins Hospital, 600 N. Wolfe
St., Baltimore, MD 21287.
4 Department of Psychiatry, University of Massachusetts Medical School, 55 Lake
Ave. N., Worcester, MA 01655.
5 Present address: Department of Radiology, Children's Hospital—Boston,
300 Longwood Ave., Boston, MA 02115.
Received December 3, 2001;
accepted after revision March 15, 2002.
Address correspondence to P.K. Kleinman.
Abstract
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MATERIALS AND METHODS. High-detail postmortem skeletal radiologic surveys of 101 neonates and infants who had died from sudden infant death syndrome were reviewed. The average age at the time of death was 2.6 months (range, 2 weeks—8 months 2 weeks). The location, distribution, and thickness of subperiosteal new bone formation of the long bones were noted and measured with an ocular magnification system.
RESULTS. subperiosteal new bone formation was identified in 35 infants (35%), all of whom were between 1 and 4 months of age. The prevalence of subperiosteal new bone formation involving one or more bones was 37% for ages 1-2 months, 55% for ages 2-3 months, and 35% for ages 3-4 months. subperiosteal new bone formation involved the tibia in 29 infants (bilateral involvement in 19) and the femurs in 14 infants (bilateral involvement in 11). The humerus was a site of subperiosteal new bone formation in 12 infants; the ulna, in seven infants; and the radius, in two infants. The thickness of the subperiosteal new bone formation was never more than 1.8 mm, and the average thickness for the various long bones ranged from 0.7 to 0.9 mm.
CONCLUSION. Our results suggest that subperiosteal new bone formation is a common finding in infants 1-4 months of age. It is potentially an abnormal finding in neonates (CI = 0.0, 0.007) and in infants older than 4 months of age (CI = 0.0, 0.003). A thickness of 2 mm or more in subperiosteal new bone formation is likely to be abnormal and should prompt further diagnostic evaluation.
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Previous studies [1,2,3] of subperiosteal new bone formation in healthy infants have provided little detail on case selection criteria, imaging protocols, and statistical analyses. Using a meticulous imaging protocol and high-detail radiographic technique, we attempted to determine the prevalence, distribution, and thickness of subperiosteal new bone formation in neonates and infants. Because, by definition, no disease or traumatic injuries are found during a thorough postmortem evaluation in victims of sudden infant death syndrome, a careful radiologic study of this population could provide useful information regarding skeletal variability in healthy neonates and infants [11,12,13,14,15,16].
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The average age of the infants at time of death was 2.6 months (range, 2 weeks—8 months 2 weeks). All the infants in our study had meticulous skeletal surveys that typically were performed with a single-emulsion, single-screen, high-detail radiographic system (Lanex Fine/Min-RM; Eastman Kodak, Rochester, NY). Images were obtained at 55 kVp with a 101.6-cm tube-to-film distance. The skeletal survey protocol included well-collimated frontal views of the appendicular skeleton and frontal and lateral views of the axial skeleton, conforming to standards of the American College of Radiology [17].
Using a handheld ocular magnifying device (Measuring Magnifier; Bausch & Lomb, Rochester, NY) with a built-in metric scale (one division = 0.1 mm), we measured subperiosteal new bone formation along the shafts of the long bones if we observed a double contour that paralleled and was distinctly separate from the underlying cortex (Fig. 1). Such bone formation was regarded as absent if the new bone appeared to be incorporating into the underlying cortex. We measured the new bone formation at a single site in the humerus, ulna, and radius and along the medial and lateral aspects of the femur and tibia. The thickest portion was measured on the frontal projections, from the most peripheral margin of the underlying cortex to the most peripheral margin of the subperiosteal new bone. We grouped the neonates and infants according to age, defining a total of five groups: younger than 1 month, from 1 month up to 2 months, from 2 months up to 3 months, from 3 months through 4 months, and older than 4 months. The prevalence and range of thickness of subperiosteal new bone formation were obtained for each group. Confidence intervals (CIs) of 95% were calculated for each group using the normal approximation of the binomial distribution for infants whose ages ranged from 1 month to 4 months. For infants younger than 1 month and older than 4 months, the Poisson distribution was used. Because tibial and femoral subperiosteal new bone formation is commonly encountered in clinical practice, we also analyzed pooled measurements for the tibias and femurs. We used the maximal thickness of the lateral or medial aspects of the tibias or femurs of each infant to calculate the distribution of the mean subperiosteal new bone formation.
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Figure 3 shows the distribution of subperiosteal new bone formation according to the bone in which it was observed. The tibia was most commonly observed to have subperiosteal new bone formation (48/105 bones, 46%), and tibial subperiosteal new bone formation was noted in the greatest number of infants (29/101, 29%). When such new bone development was present, it was bilateral in 66% of the cases. The femur was less frequently the site of subperiosteal new bone formation. Such new bone development was noted in 25 femurs (24%) in 14 (14%) of the 101 infants; it was bilateral in 79% of the cases. The humerus was a site of subperiosteal new bone formation in 17 (16%) of 105 bones in 12 (11%) of 101 infants. Radius and ulna involvement was less common.
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The thickness of the subperiosteal new bone formation ranged from 0.3 to 1.8 mm. For the tibia, the average thickness was 0.9 mm (range, 0.4-1.8 mm); for the femur, 0.8 mm (range, 0.3-1.4 mm); and for the humerus; 0.7 mm (range, 0.3-1.3 mm). When the data were pooled for the tibias and femurs, the mean maximum subperiosteal new bone formation was 0.92 mm and the standard deviation was 0.32. These results suggest that physiologic subperiosteal new bone formation of 2.0 mm or more along the lateral or medial aspects of either the femur or tibia is likely to occur in only five of 10,000 cases.
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Shopfner [2] also noted from sequential studies that subperiosteal new bone formation initially produced a hazy mineralized linear density paralleling the underlying normal cortex and that, over time, this layer became more discretely visible, producing the double contour of cortex initially described by Glaser [1]. The prevalence of subperiosteal new bone formation in at least one long bone, as reported by Glaser and other authors [2, 3], ranged from 27% to 46% in full-term infants and was as great as 78% in premature infants.
The overall prevalence in our study was 35%, a finding that is in agreement with previous studies. Although Glaser [1] reported that 78% of premature infants developed subperiosteal new bone formation, Shopfner [2] and Malmberg [18] separately reported a prevalence of 34% and 47%, respectively. The percentage reported by Malmberg may actually be inflated because he observed that many infants who showed the double contour along the long bones later developed rickets.
Serial measurements were also performed in these earlier studies. Glaser [1] conducted the longest follow-up, with monthly radiography of the long bones, wrists, and ankles until the children reached the age of 8 months. This lengthy follow-up period could account for the high prevalence of subperiosteal new bone formation in premature infants (78%) that Glaser reported because monthly screening would be more likely to pick up transient subperiosteal new bone formation than would a single examination performed in early infancy. Shopfner [2], Hancox et al. [3], and Malmberg [18] conducted more limited sequential follow-up, usually a subsequent study performed 1 month after the initial examination. Because our study was performed on postmortem subjects, sequential images were not possible nor were antemortem images available. Lack of birth history also precluded our evaluation of the differences, if any, between full-term and premature infants. In Shopfner's study, prematurity was not associated with an increased prevalence of subperiosteal new bone formation. We could not segregate the infants in our study into full-term and premature groups because gestational age was not routinely provided in the autopsy reports. However, our overall prevalence of 35% is in accord with Shopfner's findings in both full-term (35%) and premature (34%) infants.
Glaser [1] reported the presence of the double contour most frequently in the ulna (78%), followed by the radius (76%), tibia (49%), and fibula (28%). Hancox et al. [3] found the greatest prevalence of subperiosteal new bone formation in the tibia (22%), followed by the ulna (20%), fibula (12%), femur and radius (10% each), and humerus (3%). Shopfner [2] found that the femur was most commonly involved (32%), followed by the humerus (30%), tibia (29%), ulna (20%), and radius (10%). We found that subperiosteal new bone formation showed a predilection for occurring in the long bones of the lower extremity, with the tibia most commonly involved (46%), followed by the femur, humerus, ulna, and radius. This order of involvement persisted from age 1 to 3 months. We found no cases of subperiosteal new bone formation in the upper extremities in children older than 3 months.
With respect to age groups, we found the prevalence of subperiosteal new bone formation at one or more sites was greatest in infants who were between 2 and 3 months, followed by those who were between 1 and 2 months, and then by those who were between 3 and 4 months. Glaser [1] reported subperiosteal new bone formation most frequently between 3 and 4 months in premature infants. However, he found subperiosteal new bone formation at an earlier stage—by the age of 2 months—in full-term infants; he reported its disappearance at an earlier age in full-term infants as well, usually by the age of 5 months. These findings support the concept that the development of subperiosteal new bone formation peaks between 2 and 3 months of age in full-term infants.
Glaser's [1] observation of subperiosteal new bone formation in infants as old as 7 months contrasts with the findings of our study; we found no instance of subperiosteal new bone formation in infants older than 4 months. Our study found that after 4 months the new bone showed incorporation into the adjacent cortex. Possible pitfalls in earlier studies include the lack of standardized high-detail imaging techniques and the failure to reliably exclude infants with underlying diseases or inflicted trauma that might produce subperiosteal new bone formation. Our study used high-detail skeletal radiographic surveys performed in accordance with the recommendations of the American College of Radiology [17], and we excluded infants with underlying disease or traumatic injury by studying neonates and infants whose cause of death was sudden infant death syndrome. Findings of our study also disagree with those of Shopfner [2] on the bilateral nature of the findings. Shopfner stated that in no instance was subperiosteal new bone formation seen unilaterally and that it may occasionally be more prominent on one side. The use of the ocular magnifying system in our study allowed more precise measurements of subperiosteal new bone formation. We found asymmetric subperiosteal new bone formation of the long bones to be quite common, with a unilateral involvement of 58% in the humerus, 33% in the tibia, 30% in the ulna, and 24% in the femur.
The radiologic appearances of subperiosteal new bone formation at different anatomic sites vary, but they share the feature of a smooth regular band of mineralized density that is distinctly separated from the underlying cortex by a zone of radiolucency. Subperiosteal new bone that gradually blends into the underlying cortex may occasionally be seen in infants who are as old as 6 months. However, applying our strict radiologic criteria and high-detail imaging technique, we found subperiosteal new bone formation in infants older than 4 months and younger than 1 month to be an uncommon phenomenon. In our study, subperiosteal new bone formation measuring as much as 1.8 mm was a common and presumably a normal finding in infants, and in no instance was it found to exceed a thickness of 1.8 mm.
In summary, subperiosteal new bone formation is a relatively common finding in infants between 1 and 4 months of age; such bone formation peaks between 2 and 3 months. subperiosteal new bone formation presumably represents a normal physiologic pattern of rapid bone growth by intramembranous ossification resulting in a double cortical layer that is progressively incorporated into the preexisting underlying cortex. Although subperiosteal new bone formation tends to involve the long bones bilaterally, unilateral involvement is common. subperiosteal new bone formation is seen most often in the tibia, followed by the femur, humerus, ulna, and radius. The presence of clearly definable subperiosteal new bone formation in infants older than 4 months or with a thickness exceeding 2 mm should be viewed as sign of potential abnormality.
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= total number of
infants in age group, 
= number of infants in age group with
subperiosteal new bone formation, [UNK] = number of infants with subperiosteal
new bone formation in multiple sites.