New radiographic standards for age at appearance of the ossification center of the femoral head in Japanese: Appearance at ≤12 months of age is normal in Japanese infants

New radiographic standards for age at appearance of the ossification center of the femoral head in Japanese: Appearance at ≤12 months of age is normal in Japanese infants

Journal of Orthopaedic Science xxx (2018) 1e4 Contents lists available at ScienceDirect Journal of Orthopaedic Science journal homepage: http://www...

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Journal of Orthopaedic Science xxx (2018) 1e4

Contents lists available at ScienceDirect

Journal of Orthopaedic Science journal homepage: http://www.elsevier.com/locate/jos

Original Article

New radiographic standards for age at appearance of the ossification center of the femoral head in Japanese: Appearance at 12 months of age is normal in Japanese infants Ryo Sugawara a, *, Hideaki Watanabe b, Naoya Taki b, Toshinori Aihara c, Rieko Furukawa c, Waka Nakata c, Katsushi Takeshita a, Ichiro Kikkawa b a b c

Department of Orthopedic Surgery, Jichi Medical University, 3311-1 Yakushiji, Shimotsuke, Tochigi, 329-0498, Japan Department of Pediatric Orthopedic Surgery, Jichi Children's Medical Center Tochigi, 3311-1 Yakushiji, Shimotsuke, Tochigi, 329-0498, Japan Department of Pediatric Medical Imaging, Jichi Children's Medical Center Tochigi, 3311-1 Yakushiji, Shimotsuke, Tochigi, 329-0498, Japan

a r t i c l e i n f o

a b s t r a c t

Article history: Received 13 June 2018 Received in revised form 9 August 2018 Accepted 26 August 2018 Available online xxx

Background: The ossification center of the femoral head reportedly appears at 7e8 months in 95% infants in the radiographs, but its appearance often delays in Japanese normal infants. The purpose of this study was to survey the age at appearance of the femoral head in the radiographs, evaluate the normal standards of its appearance in Japanese infants, and determine whether the acetabular state affects the time of its appearance. Materials and methods: The patients comprised 436 infants consulted with our institution because of a limitation of abduction in flexion (LA), acetabular dysplasia, or suspected developmental dysplasia of the hip (DDH). Among these patients, 111 infants (222 hips) without radiographic appearance of the femoral head at the first visit were reviewed. The 222 hips were classified into three groups: a angle 30 (DDH þ group), <30 with LA (DDH-/LA þ group), or < 30 without LA (DDH-/LA-group). The age at appearance of the femoral head was investigated in the radiograph in each group. Results: The 50th percentile of the age at appearance of the femoral head was 6 months in the DDH-/LAand DDH-/LA þ groups and 8 months in the DDH þ group. The femoral head significantly appeared earlier in the DDH-/LA- and DDH-/LA þ groups than in the DDH þ group (P < 0.01). The 95th percentile was 12 months in all groups. Conclusions: Radiographic appearance of the ossification center of the femoral head by 12 months of age is normal in Japanese infants. When the a angle is  30 , the age at appearance of the femoral head is sometimes delayed. © 2018 The Japanese Orthopaedic Association. Published by Elsevier B.V. All rights reserved.

1. Introduction As an indicator of growth maturation, bone age has been radiographically evaluated for many years. The hand is used in children of all ages because of its numerous secondary ossification centers in the phalanges and metacarpals, and the knee or foot is used in children younger than 2 years of age [1]. The femoral head, which reportedly appears at 2e3 weeks after birth in some infants, at 4 months in 50%, and at 7e8 months in 95% [2], is also an important radiographic landmark in infants. The appearance of the

* Corresponding author. Fax: þ81 285 44 1301. E-mail address: [email protected] (R. Sugawara).

ossification center of the femoral head is delayed in infants with skeletal dysplasia, endocrine diseases such as cretinism, and developmental dysplasia of the hip (DDH) [3]. Therefore, a delay in the appearance of the femoral head is an important finding that should not be overlooked to detect medical problems that cause growth retardation and DDH. In Japan, orthopedists and pediatricians have an opportunity to examine the infant's hip at the 4-month health checkup, and radiographs are frequently performed when DDH is suspected. The femoral head is often radiographically absent at the 4-month checkup, and it remains absent in some infants even at 7e8 months of age (Fig. 1). In Japan, mass screening for congenital metabolic disorders such as cretinism is performed in 97% of newborns [4], and DDH or skeletal dysplasia is easily detected in

https://doi.org/10.1016/j.jos.2018.08.017 0949-2658/© 2018 The Japanese Orthopaedic Association. Published by Elsevier B.V. All rights reserved.

Please cite this article in press as: Sugawara R, et al., New radiographic standards for age at appearance of the ossification center of the femoral head in Japanese: Appearance at 12 months of age is normal in Japanese infants, Journal of Orthopaedic Science (2018), https://doi.org/ 10.1016/j.jos.2018.08.017

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R. Sugawara et al. / Journal of Orthopaedic Science xxx (2018) 1e4

limitation of abduction in flexion (LA), acetabular dysplasia, or DDH/suspected DDH. The inclusion criteria of this study were 1) radiographic absence of the bilateral ossification center of the femoral head at the first consultation and 2) radiographic appearance of the bilateral femoral head during the serial checkup (after 1 to 3 months from the previous checkup). The exclusion criteria were 1) hip dislocation, 2) hip dysplasia with an a angle of 30 treated with a Pavlik harness because of a larger tear drop distance on the affected side, and 3) medical problems causing the growth retardation. In total, 111 infants (222 hips) who met these criteria were retrospectively reviewed (Fig. 2). Eighty-five infants were female and 26 were male, with a mean age of 3.6 months at the time of the first visit. Sixty-five infants were LA (unilateral 60, bilateral 5) and 46 were acetabular dysplasia (unilateral 39, bilateral 7), which included 99 of non-affected side. The 222 hips were classified into 3 groups: the a angle [6] of 30 (DDH þ group), <30 with LA (DDH-/LA þ group), or <30 without LA (DDH-/LA-group). The age at appearance of the femoral head, the a angle, and the OE angle [7] (the angle defined by point O and E, see Fig. 3) at the first visit were investigated in the radiographs in each group. In addition, the 50th percentile for the age at appearance of the femoral head was calculated; hips below the 50th percentile were classified as the early-appearance (Group E), and those above this percentile were classified as the lateappearance (Group L). The a and OE angles at the first visit were compared between Groups E and L in each of the two groups. Software (SPSS ver. 22; IBM Corp., Armonk, NY, USA) was used for statistical analysis. The age at appearance of the femoral head was compared among the DDHþ and normal groups using the ManneWhitney U test, and the a and OE angles were compared between Groups E and L using the paired t-test. The accepted level of significance was a P value of <0.05. 3. Results

Fig. 1. The radiographs of a girl without history of growth retardation. (a) At 9 months of age. (b) The ossification center of the femoral head appeared at 16 months of age at last.

the radiographs because of its abnormal configuration. Therefore, most infants without the appearance of the femoral head may have no medical problems. We often have difficulty making clinical decisions in infants without the femoral head in the radiographs at 7e8 months of age. In the previous study of Sugawara et al. [5], we subsequently noticed a delay in the appearance of the femoral head in infants with DDH compared with this previous report. The results indicated that the age at appearance of the femoral head in Japanese infants might differ from the previously reported age. In addition, considering the delayed appearance of the femoral head in infants with DDH, we speculate that the acetabular state affects the time of the appearance of the femoral head. The purpose of this study was to survey the age at appearance of the femoral head on radiographs, evaluate the normal standards of its appearance in Japanese infants, and determine whether the acetabular state affects the time of its appearance.

Of the 222 hips, 99 (26 left, 73 right) were classified as the DDH-/LA-group, 70 (51 left, 19 right) as the DDH-/LA þ group, and 53 (34 left, 19 right) as the DDH þ group. The femoral head began to appear at 3, 3, and 4 months in the DDH-/LA-, DDH-/LAþ, and DDH þ groups, respectively. The median value (50th percentile) of the age at appearance of the femoral head was 6 months in the DDH-/LA- and DDH-/LA þ groups and 8 months in the DDH þ group (Figs. 4e6). The femoral head appeared significantly earlier in the DDH-/LA- and DDH-/LA þ groups than in the DDH þ group (P < 0.01) (Table 1). In addition, the 95th

2. Materials and methods This retrospective comparative study was performed with approval from the ethics committee of our institution. The patients comprised 436 infants aged <8 months whose parents consulted with our institution from October 2006 to March 2014 because of a

Fig. 2. Flow diagram of patients in this study.

Please cite this article in press as: Sugawara R, et al., New radiographic standards for age at appearance of the ossification center of the femoral head in Japanese: Appearance at 12 months of age is normal in Japanese infants, Journal of Orthopaedic Science (2018), https://doi.org/ 10.1016/j.jos.2018.08.017

R. Sugawara et al. / Journal of Orthopaedic Science xxx (2018) 1e4

Fig. 3. Radiographic measurements. The a angle is defined as the angle subtended by Y-line and point E. The OE angle is defined as the angle subtended by a vertical line originating from point O and point E.

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Fig. 6. Age at appearance of the DDH þ group. The 50th percentile was 8 months, and the 95th percentile was 12 months. DDH: Developmental Dysplasia of the Hip, LA: Limitation of Abduction.

difference was observed in the a or OE angle at the first visit between Groups E and L in any of the three groups (Table 2).

4. Discussion

Fig. 4. Age at appearance of the DDH-/LA-group. The 50th percentile was 6 months, and the 95th percentile was 12 months. DDH: Developmental Dysplasia of the Hip, LA: Limitation of Abduction.

Fig. 5. Age at appearance of the DDH-/LA þ group. The 50th percentile was 6 months, and the 95th percentile was 12 months. DDH: Developmental Dysplasia of the Hip, LA: Limitation of Abduction.

percentile was 12 months in all groups. The most delayed appearance was observed at 18 months of age in both the DDH-/LA- and DDH-/LA þ groups and at 16 months in the DDH þ group. In the DDH-/LA-group, the a angle in Groups E and L was 25.0 ± 4.4 and 25.3 ± 3.9 , and the OE angle in the two groups was 6.0 ± 3.9 and 7.3 ± 5.0 , respectively. In the DDH-/LA þ group, the a angle in Groups E and L was 25.9 ± 4.6 and 25.6 ± 5.7, and the OE angle in the two groups was 4.8 ± 5.7 and 6.7 ± 5.0 , respectively. In the DDH þ group, the a angle in Groups E and L was 33.0 ± 5.3 and 33.8 ± 6.1, and the OE angle in the two groups was 1.9 ± 5.5 and 0.8 ± 7.6 , respectively. No significant

The ossification center of the femoral head is reportedly present radiographically in 50% of infants at 4 months of age and in 95% at 7e8 months of age [2,8,9]. However, in the present study, the 95th percentile for the age at appearance of the femoral head was 12 months in Japanese infants. The 50th percentile was 6 months in the DDH-/LA- and DDH-/LA þ groups and 8 months in the DDH þ group, showing that the age at appearance of the femoral head in Japanese infants was particularly delayed when the a angle was 30 . Based on these findings, the radiographic appearance of the femoral head at 12 months of age may be normal, and it is not necessary to suspect the presence of medical problems causing growth retardation unless the height or weight is lower than the standard deviation of the growth curve. The reason for the late appearance of the femoral head in this study compared with previous reports is unclear. Differences in the age of the appearance of the femoral head among nations or populations have been reported [1,10,11], and the nutritional state, pediatric health care, and race-associated growth variations have been suggested as reasons. Because a previous study showed faster maturity in Negroid than Caucasoid races [1], Mongoloid individuals with a smaller physique may mature slower than the other races. In this study, the femoral head appeared later in the DDH þ group, indicating that an a angle of 30 is associated with its late appearance. However, the a and OE angles did not significantly differ between Groups E and L in each group. The reason for the late appearance of the femoral head with a larger a angle is unclear. Matsushita et al. [12] reported femoral head enlargement after reduction using the extensive anterolateral approach in patients with DDH, suggesting that the acetabulum and femoral head grow well when the femoral head is set in a concentrically reduced position. Therefore, even before the appearance of the ossification center of the femoral head, poor concentricity with hip dislocation or an a angle of 30 causes delayed growth of the femoral head, resulting in a delay in the appearance of the femoral head. No studies have focused on the timing of the radiological appearance of the ossification center of the femoral head, particularly in Japanese; therefore, the results of this study may provide normal standards for Japanese infants. These standards may be important findings that orthopedists, pediatricians, and radiologists need to know to avoid further invasive examinations for suspected medical problems and prevent anxiety in the infants’

Please cite this article in press as: Sugawara R, et al., New radiographic standards for age at appearance of the ossification center of the femoral head in Japanese: Appearance at 12 months of age is normal in Japanese infants, Journal of Orthopaedic Science (2018), https://doi.org/ 10.1016/j.jos.2018.08.017

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R. Sugawara et al. / Journal of Orthopaedic Science xxx (2018) 1e4

Table 1 The median value (50th percentile) of radiographic age at appearance of the ossification center of the femoral head in each group.

P value

month after birth

DDH-/LA- group

6 0.42

DDH-/LA+ group

6

<0.01* <0.01*

DDH+ group

8

*: significant difference DDH: Developmental Dysplasia of the Hip LA: Limitation of Abduction

Table 2 The a and OE angles at the first visit in the early and late appearance group.

DDH-/LA- group DDH-/LA þ group DDH þ group

a angle OE angle a angle OE angle a angle OE angle

Early appearance (Group E)

Late appearance (Group L)

P value

25.0 ± 4.4 6.0 ± 3.9 25.9 ± 4.6 4.8 ± 5.7 33.0 ± 5.3 1.9 ± 5.5

25.3 ± 3.9 7.3 ± 5.0 25.6 ± 5.7 6.7 ± 5.0 33.8 ± 6.1 0.8 ± 7.6

0.77 0.16 0.79 0.15 0.64 0.56

OE angle: the angle defined by point O and E, see Fig. 3. DDH: Developmental Dysplasia of the Hip. LA: Limitation of Abduction.

families. In recent years, ultrasonography has been commonly used because of its convenience and noninvasiveness for hip screening in infants, whereas radiographic evaluation is underestimated because of its radiation exposure. However, even at present, radiographic evaluation remains the gold standard for bone evaluation because the reproducibility is high and follow-up with growth is easily possible. In addition, simultaneous evaluation of the hip is possible with radiographic examination of the chest and abdomen, and the numbers of institutions allowing low-dose radiographic examination have been increasing. Therefore, radiographic evaluation will also be useful in the future, and the findings in this study are clinically important and necessary. The limitations of this study are as follows: 1) chronological age instead of gestational age was used for the age at appearance of the femoral head; 2) we did not consider factors that might affect the age at appearance, such as nutritional state, height, and weight; and 3) serial radiographs were not obtained every month because of frequent radiation exposure. In conclusion, radiographic appearance of the ossification center of the femoral head by 12 months of age is normal in Japanese infants. When the a angle is  30 , the age at appearance of the femoral head is sometimes delayed, but its association is unclear.

Conflict of interest The authors declare that they have no conflict of interest. References [1] Kan JH, Strouse PJ. Embryology, anatomy, and normal findings. In: Coley BD, editor. Caffey's pediatric diagnostic imaging. 12th ed. Philadelphia PA: Elsevier Saunders; 2013. p. 1327e46. [2] Garn SM, Rohmann CG, Silverman FN. Radiographic standards for postnatal ossification and tooth calcification. Med Radiogr Photogr 1967;43(2):45e66. [3] Bertol P, Macnicol MF, Mitchell GP. Radiographic features of neonatal congenital dislocation of the hip. J Bone Joint Surg Br 1982 Feb;64(2):176e9. [4] Present status of maternal and child health e Ministry of health, labour and welfare, (in Japanese). http://www.mhlw.go.jp/stf/shingi/2r9852000001oujoatt/2r9852000001oumv.pdf, Accessed October 12 2017. [5] Sugawara R, Watanabe H, Hagiwara K, Inoue H, Takeshita K, Kikkawa I. Radiological results of treatment using an extensive anterolateral approach for developmental dysplasia of the hip: minimum 5-year follow-up. J Pediatr Orthop B 2016 Nov;25(6):499e503. [6] Yamamuro T, Chene SH. A radiological study on the development of the hip joint in normal infants. Nippon Seikeigekagakkai Zasshi (J Jpn Orthop Assoc.) 1975 Jul;49(7):421e39 (in Japanese). [7] Ohmori T, Endo H, Mitani S, Miyanaga H, Tetsunaga T, Ozaki T. Radiographic prediction of the results of long-term treatment with the Pavlik harness for developmental dislocation of the hip. Acta Med Okayama 2009 Jun;63(3): 123e8. [8] Scoles PV, Boyd A, Jones PK. Roentgenographic parameters of the normal hip. J Pediatr Orthop 1987 Nov-Dec;7(6):656e63. [9] Segal LS, Schneider DJ, Berlin JM, Bruno A, Davis BR, Jacobs CR. The contribution of the ossific nucleus to the structural stiffness of the capital femoral epiphysis: a porcine model for DDH. J Pediatr Orthop 1999 Jul-Aug;19(4): 433e7. [10] Pettersson H, Theander G. Ossification of femoral head in infancy. I. Normal Standards. Acta Radiol Diagn 1979;20(1):170e9. [11] Paranjape M, Cziger A, Katz K. Ossification of femoral head: normal sonographic standards. J Pediatr Orthop 2002 Mar-Apr;22(2):217e8. [12] Matsushita T, Miyake Y, Akazawa H, Eguchi S, Takahashi Y. Open reduction for congenital dislocation of the hip: comparison of the long-term results of the wide exposure method and Ludloff's method. J Orthop Sci 1999 Sep;4(5): 333e41.

Please cite this article in press as: Sugawara R, et al., New radiographic standards for age at appearance of the ossification center of the femoral head in Japanese: Appearance at 12 months of age is normal in Japanese infants, Journal of Orthopaedic Science (2018), https://doi.org/ 10.1016/j.jos.2018.08.017