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Published online before print August 26, 2002, 10.1148/radiol.2251011130
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(Radiology 2002;225:240-244.)
© RSNA, 2002

Pediatric Imaging

Ossification Sequence in Infants Who Die during the Perinatal Period: Population-based References1

Øystein E. Olsen, MD, Rolv T. Lie, PhD, Ralph S. Lachman, MD, Helga Maartmann-Moe, MD and Karen Rosendahl, MD, PhD

1 From the Departments of Radiology (Ø.E.O., K.R.) and Pathology (H.M.M.), Haukeland University Hospital, Bergen, Norway; Section for Medical Statistics and Medical Birth Registry of Norway, University of Bergen, Norway (R.T.L.); and International Skeletal Dysplasia Registry, Cedars-Sinai Medical Center, Los Angeles, Calif (R.S.L.). Received June 28, 2001; revision requested August 16; revision received October 1; accepted April 25, 2002. Supported by the Sigrun and Haakon Ødegaard Foundation. Address correspondence to Ø.E.O., Department of Radiology, Great Ormond Street Hospital for Children, Great Ormond St, London WC1N 3JH, England (e-mail: oeol@start.no).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To determine population-based references for the relationships between the presence of ossification centers and gestational age and skeletal length measurements among infants who die during the perinatal period, as well as to evaluate the possible influence of intrauterine growth restriction on ossification stage.

MATERIALS AND METHODS: During an 11-year period, nearly all infants who died perinatally in a well-defined geographic area routinely underwent radiography with a standardized technique. The presence of visible secondary ossification centers in the singletons (n = 495) was evaluated. Cluster analysis was used to identify stages of ossification; a sequential appearance of secondary ossification centers was assumed. Comparisons were made with Wilks {lambda} between male and female infants and between infants who were presumed to have growth restriction and those who were not. Reference ranges for the presence of ossification centers were calculated for interquartile ranges of femur length and gestational age.

RESULTS: Eight clusters of ossification defining different stages of ossification of the pelvis, hindfeet, and knees were identified. The sequential clusters outlined well-defined intervals of femur length and gestational age. Bone lengths, birth weight, and gestational age within ossification clusters did not differ between the sexes (Wilks {lambda} = 0.989, P = .532) or according to whether growth restriction was presumed to exist (Wilks {lambda} = 0.958, P = .481).

CONCLUSION: The reference diagrams calculated with this method indicate relationships between ossification sequence and both gestational age and skeletal length measurements.

© RSNA, 2002

Index terms: Bones, growth and development • Fetus, death • Fetus, skeletal system • Radiography, in infants and children, 44.11, 45.11, 46.11


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Postmortem full-body radiography has been suggested as a routine supplement to autopsy in infants who die during the perinatal period (1). Radiography is considered valuable for diagnosing various syndromes and skeletal dysplasias as well as for assessing fetal development (1–4). A reference describing fetal skeletal developmental stages might aid these purposes. Delayed epiphyseal ossification is an expression of several congenital syndromes and dysplasias. A search of the POSSUM database (version 5.1; Murdoch Institute, Melbourne, Australia) yielded a list of 131 syndromes when the keywords "delayed ossification of epiphyses" were entered. Marked delay of ossification is seen in various skeletal dysplasias and is characteristic of type II collagenopathies such as spondyloepiphyseal dysplasia congenita and achondrogenesis type II-hypochondrogenesis (5).

It has also been generally thought that the sequence of ossification is less subject to influence by intrauterine growth restriction than is skeletal length growth (6), but substantial evidence for this is missing. Some studies on fetal ossification exist (6–10). However, these are neither population-based nor do they cover the whole fetal period of current interest. To the best of our knowledge, the appearance of calcified ossification centers in relation to both gestational age and the sizes of long bones has thus not been firmly established.

The purpose of our study was to determine population-based references for the relationships between the presence of ossification centers and both gestational age and skeletal length measurements among infants who die during the perinatal period, as well as to evaluate the possible influence of intrauterine growth restriction on ossification stage.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Infants who died during the perinatal period (ie, from a gestational age of 16 weeks to 7 days after delivery) in Haukeland University Hospital in Bergen, Norway between January 1988 and December 1998 routinely underwent postmortem examination in accordance with a standard autopsy protocol. Fetuses aborted for nonmedical reasons were not examined; this resulted in a total of 1,024 examinations. In all cases, routine full-body radiographs were obtained with a Faxitron (Faxitron X-Ray, Wheeling, Ill) apparatus, fine-grain film (Kodak XMA; Eastman Kodak, Rochester, NY), and a low-kilovolt technique. In accordance with a protocol described in the literature (11), two anteroposterior radiographs were obtained with the infant lying flat on the film with extremities extended. One radiograph was obtained for depiction of the axial skeleton, and the other (obtained with 10 fewer kilovolts) was obtained for depiction of the extremities. Additionally, one lateral radiograph was obtained with the infant in the decubitus position.

We included only cases in which the mother resided in the local Bergen, Norway, hospital area at the time of abortion or delivery. Because Haukeland University Hospital is the only maternity hospital in the area, this was thought to minimize referral bias and thereby define a population-based data set. The total population in the local hospital area was approximately 316,000 in January 2000. The population level was practically stationary during the study period. From this area, a total of 777 cases of perinatal death were reported to the Medical Birth Registry of Norway during the study period. We were able to access the records of 542 (70%) of these cases. The missing cases probably represented fetuses that were aborted for nonmedical indications and did not undergo autopsy. Forty-seven (9%) of the 542 infants were twins. Twins were excluded from our study because the number was too small to allow calculation of separate references.

Of the 495 remaining infants, 352 (71%) had died in utero at a mean gestational age of 24.4 weeks ± 7.6 (SD), 65 (13%) had been subject to procured abortion, and 52 (11%) had died in the early neonatal period. In 26 (5%) infants, the time of death was unknown. One hundred eighty-four (37%) of the infants were female, 306 (62%) were male, and five (1%) were of unknown or uncertain sex. Physicians at our maternity ward obtained information on maternal health, pregnancy, and birth history from clinical records. Relevant information (ie, findings in the fetus or neonate and placenta at autopsy, chromosomal findings, and final diagnosis) was collected by one of the authors (H.M.M.) from autopsy reports. Information on birth weight and gestational age as estimated from the mother’s last menstrual period was obtained from the records of the Medical Birth Registry of Norway.

Our institutional review board did not require its approval or informed consent for this study.

One of the authors (Ø.E.O.) evaluated the presence of ossification centers without knowledge of actual gestational age. The number of radiographically visible secondary ossification centers in the hindfeet and knees and the existence of ossification of the ischial rami and superior pubic rami were noted. These regions undergo secondary ossification during the second and third trimesters and were reliably depicted on the radiographs. The evaluation of ossification centers was performed directly with the original radiographs. Examples of different ossification centers are shown in Figure 1. Radiographic anthropometric measurements of humerus, radius, femur, tibia, and lumbar spine lengths had been performed in an earlier study (12); these measurements were used in some of the analyses in the present study.



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  		Figure 1. Portions of radiographs in different fetuses show ossification centers of interest in the perinatal period. Upper left: Both ischial rami (*) and one superior pubic ramus (arrow) are visible. Lower left: Two ossification centers (arrows) are visible in the hindfoot. Right: Two ossification centers (arrows) are visible in the knee.

 
We grouped the subjects according to a higher or lower suspicion of growth restriction based on probability. Infants with probable growth restriction were identified through reports of placental abnormality, any abnormal findings at autopsy, chromosomal anomalies, and/or clinical suspicion of growth restriction. According to these criteria, 344 (69%) of the 495 infants were categorized as having high probability of growth restriction; 151 (31%) were categorized as having low probability.

To reduce the effects of inaccurate individual measurements, we calculated a mean length variable, which was defined as the mean of the lengths of the humerus, radius, femur, tibia, and lumbar spine. Gestational age was calculated as the duration in weeks from the first day of the last menstrual period, rounded to the nearest whole week. Reference curves for femur length were taken from an earlier study based on the same material (12).

For statistical analysis, we used SPSS for Windows (release 9; SPSS, Chicago, Ill). To select appropriate ossification stages for further analyses, we performed a K-means cluster analysis (based on manufacturer’s recommendation in SPSS [r] base 9.0 applications guide. Chicago: SPSS, 1999), with the number of ossification centers in the hindfeet, knees, and pelvis as discriminating variables. We decided that use of eight clusters would confer an appropriate degree of refinement for our purposes. The clusters were ordered according to the means of the mean length variable within each cluster. For gestational age, weight, mean length, and the ratio of weight to mean length within these ossification clusters, we tested for any significant correlation with sex and suspicion of growth restriction. This was performed with multivariate tests, including Wilks {lambda}. The Spearman {rho} was used to test the correlation between ossification clusters and gestational age, birth weight, and bone lengths. To obtain reference ranges for gestational age and femur length within ossification clusters, we chose to plot median values and 25th- and 75th-percentile ranges with the Tukey test because of a nonnormal distribution of data. The {alpha} level was set at .05. All reported P values are two-tailed.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Descriptions of the eight secondary ossification clusters as they included ossification centers in the ischial rami, superior pubic rami, hindfeet, and knees are provided in the Table. The cluster sequence correlated with femur, tibia, humerus, radius, and lumbar spine lengths; birth weight; and gestational age ({rho} = 0.78–0.87, P < .001). No sex differences were found for birth weight, ratio of weight to mean length, gestational age, or the mean length variable within ossification clusters (Wilks {lambda} = 0.989, P = .532). Therefore, we decided to pool data from the sexes in our description. Sixteen (3%) of the 495 cases could not be classified according to the eight cluster descriptions.


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  		Ossification Clusters

 
Figure 2 demonstrates the association between ossification stages and both gestational age and femur length. A reference plot (12) for femur length by gestational age was overlain after these data were plotted. As shown, the 25th- and 75th-percentile ranges of femur length and gestational age within ossification stages are principally seen within the 10th- and 90th-percentile curves of femur length by gestational age. This applies in particular to the plot of ossification clusters, where the train of interquartile ranges also nearly covers the whole ranges of gestational ages and femur lengths.



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  		Figure 2. Graphs show the median and Tukey test values for gestational age and femur length within ossification stages. Dotted overlays represent mean and 10th-, 25th-, 75th- and 90th-percentile ranges of femur length by gestational age calculated earlier from the same data. w = weeks. Upper left: Ossification stages in pelvis by gestational age ({rho} = 0.737, P < .001) and femur length ({rho} = 0.761, P < .001). 0 = neither ischial rami nor superior pubic rami ossified, 1 = one or both ischial rami but no superior pubic ramus ossified, 2 = both ischial rami and at least one superior pubic ramus ossified. Upper right: Ossification stages in hindfeet by gestational age ({rho} = 0.674, P < .001) and femur length ({rho} = 0.735, P < .001). 0 = no hindfoot ossification centers visible, 1 = one visible ossification center in at least one hindfoot, 2 = two visible centers in at least one hindfoot, 3 = three visible centers in at least one hindfoot. Lower left: Ossification stages in knees by gestational age ({rho} = 0.546, P < .001) and femur length ({rho} = 0.573, P < .001). 0 = no knee ossification centers visible, 1 = one visible ossification center in at least one knee, 2 = two visible centers in at least one knee. Lower right: Ossification clusters by gestational age ({rho} = 0.783, P < .001) and femur length ({rho} = 0.871, P < .001). See Table for cluster definitions.

 
To identify possible effects of abnormally retarded growth within clusters of ossification stage, we plotted gestational age, mean length variable, birth weight, and ratio of weight to mean length by ossification cluster separately according to high and low suspicions of growth restriction (Fig 3). Delayed ossification following growth restriction would result in higher gestational age among growth-restricted infants than in non–growth-restricted infants within the same ossification cluster. Moreover, dissociation between secondary ossification and bone lengths would result in different bone lengths within ossification clusters. Figure 3 shows, on the contrary, that within ossification clusters the mean values in the two groups were almost equal, with the 95% CIs considerably overlapping. There were no significant effects of suspected growth restriction on femur, tibia, humerus, radius, or lumbar spine lengths; birth weight; ratio of weight to mean length; or gestational age within ossification clusters (Wilks {lambda} = 0.958, P = .481).



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  		Figure 3. Graphs show ossification clusters among infants with lower ({bullet}) and higher ({circ}) probability of growth restriction by gestational age (upper left), weight (upper right), mean length variable (ie, the arithmetic mean of humerus, radius, femur, tibia, and lumbar spine lengths) (lower left), and ratio of weight to mean length (lower right). The two groups did not differ (Wilks {lambda} = 0.958, P = .481). See Table for cluster definitions. w = weeks.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
We present interquartile values for skeletal length measurements and gestational age within eight clusters defined by radiographically visible ossification centers in the pelvis, hindfeet, and knees. For graphic presentation of the main results, we chose gestational age and femur length for the axes because these two parameters are commonly used. The interquartile ranges, according to both gestational age and femur length, were principally seen within the boundaries of a femur-length–by–gestational-age reference curve, which had been calculated earlier based on the same data. Some degree of overstepping of the outer reference lines and some gapping between interquartile bars were seen. This was probably due to the wide ranges of femur lengths and gestational ages within single ossification stages (eg, after 23 weeks of gestation, nearly all the infants had ossification of both the ischial rami and the superior pubic rami; this stage of ossification was maintained throughout gestation). Gapping was almost eliminated by plotting pelvic, hindfeet, and knee ossification stages together in categories according to precalculated clusters. The exact number of clusters was decided a priori, and the number of eight was used to permit an appropriate degree of separation. The use of cluster analysis presupposes a stepwise appearance of ossification centers. We sorted the ossification clusters by skeletal length measurements, which might theoretically be risky due to assumptions of longitudinal relationships that could not be derived from our truly cross-sectional material. However, for practical purposes this was not considered controversial.

Some previous researchers have aimed at selecting "normal" infants from among those who died perinatally (6,11). We considered this inappropriate because perinatal death is not normal and conditions affecting infants who die in the perinatal period probably represent a broad spectrum of abnormality. The term normal therefore would only be applied to infants in whom available methods were unable to reveal the cause of death. We chose instead to include all infants from a geographically well-defined area who died in the perinatal period, thereby establishing a population-based data set. From this data set we calculated quartiles to describe skeletal size and gestational age for the majority of infants within different ossification stages.

The term intrauterine growth restriction (or retardation) is commonly used in describing fetuses that are smaller than is appropriate for their estimated gestational age. The diagnosis is based on various measurements, is flawed by methodologic difficulties, and entails a high degree of uncertainty. We separated our study population into groups of higher and lower probability for growth restriction on the basis of clinical suspicion. Given that growth restriction was more frequently seen in "short-for-age" infants rather than in infants with delayed ossification, one would expect to see divergent length measurements within the same ossification stages between these two groups.

On the contrary, when we compared the two groups in terms of the distribution of bone lengths, gestational age, and weight within ossification clusters, we did not see any effect of probable growth restriction. The SDs of the mean length variable within ossification clusters ranged from 4 to 9 mm. Assuming that a clinically interesting difference would be 5 mm, the statistical power for detecting an overall effect would be around 85%, given a standardized difference of 0.56 and a group size of 132 (13). Additionally, the direction of differences between group means seemed coincidental, and the 95% CIs overlapped. This might indicate that there is no overall effect of growth restriction on the sequence of ossification in proportion to skeletal length measurements. For the relationship between ossification sequence and gestational age, this inference is not equally evident because considerable uncertainty is associated with the menstrual method. Further, it has been suggested that marked fetal abnormalities may be associated with even more erroneous calculations of gestational age, probably because of the increased risk of bleeding that mimics menstruation in early pregnancy (14).

On the other hand, use of the gestational age estimated at ultrasonography (US) would be even more dubious methodologically because this method itself is based on anthropometric parameters. Also, there is some evidence that the US method, even more than the menstrual method, may result in underestimations of gestational age in abnormal fetuses (15).

Several limitations apply in the interpretation of our results. To some extent, we chose to present the results as if describing a sequential process, even though our data were truly cross sectional. Therefore, our descriptions are valid for comparison only with similar subjects (ie, infants who die at specific stages in the perinatal period). The retrospective nature of our study probably introduced some uncertainty. For instance, we were not able to determine confidently the occurrence or degree of growth restriction among the infants. The rough probability method we used was thought to justify estimation of an overall effect of suspected growth restriction in our series. Description of subgroups of growth-restricted fetuses was, however, not possible.

In conclusion, no differences were seen between male and female infants or between those in whom growth restriction was suspected and those in whom it was not suspected. References are proposed for a fetal ossification stage sequence, calculated from a population-based sample of singleton infants who died perinatally.


   ACKNOWLEDGMENTS
 
We thank the Medical Birth Registry of Norway and collaborators at the Department of Obstetrics and Gynecology of Haukeland University Hospital for data access and help with data acquisition.


   FOOTNOTES
 
Author contributions: Guarantor of integrity of entire study, Ø.E.O., study concepts, Ø.E.O., R.S.L., K.R.; study design, Ø.E.O., R.T.L., R.S.L., K.R.; literature research, Ø.E.O.; clinical studies, all authors; data acquisition, Ø.E.O., H.M.M.; data analysis/interpretation, Ø.E.O., R.T.L.; statistical analysis, Ø.E.O., R.T.L.; manuscript preparation, Ø.E.O.; manuscript definition of intellectual content, editing, revision/review, and final version approval, all authors.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  8. Chan WF, Ang AH, Soo YS. The value of lower limb ossification centres in the radiological estimation of fetal maturity. Aust N Z J Obstet Gynaecol 1972; 12:55-58.[Medline]
  9. Pryse Davies J, Smitham JH, Napier KA. Factors influencing development of secondary ossification centres in the fetus and newborn: a postmortem radiological study. Arch Dis Child 1974; 49:425-431.[Medline]
  10. Kuhns LR, Finnstrom O. New standards of ossification of the newborn. Radiology 1976; 119:655-660.[Abstract]
  11. Seppanen U. The value of perinatal post-mortem radiography: experience of 514 cases. Ann Clin Res 1985; 7((suppl)44):1-59.
  12. Olsen ØE, Lie RT, Maartman-Moe H, Pirhonen J, Lachman RS, Rosendahl K. Skeletal measurements among infants who die during the perinatal period: new population-based reference. Pediatr Radiol; (in press).
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