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Kwong Et Al 2014 Skeletal Development of The Proximal Humerus in The Pediatric Population Mri Features
Kwong Et Al 2014 Skeletal Development of The Proximal Humerus in The Pediatric Population Mri Features
Kwong et al.
MRI of Proximal Humerus in Children
Pediatric Imaging
Original Research
O
ver the past few decades, there skeletal maturity [3] and the sequential de-
has been a tremendous increase velopment of the elbow and ankle joints [4,
in the use of MRI of the shoulder 5]. However, aside from a few articles that
in the pediatric patient popula- briefly describe the developing shoulder
Keywords: development, growth plate, MRI, ossification
tion. MRI of the shoulder in the infant and [6–8], there has not been, to the best of our
center, pitfalls, proximal humerus
young child is particularly useful for assess- knowledge, a comprehensive and detailed
DOI:10.2214/AJR.13.10711 ing brachial plexus injuries, infections, and MRI study of the sequential skeletal matu-
tumors. In older children and adolescents, in- ration of the proximal humerus in the pe-
Received February 2, 2013; accepted after revision creased athletic activities and increased inci- diatric age group. Familiarity is paramount
May 15, 2013.
dence of sports-related injuries have led to for accurate interpretation of shoulder MRI
1 growing use of the modality for detecting in- studies and for differentiating normal skele-
School of Medicine, NYU Langone Medical Center, 550
1st Ave, New York, NY 10016. Address correspondence to traarticular shoulder derangements, such as tal growth from disease. The purpose of our
S. Kwong (steven.kwong@med.nyu.edu). labral injuries and osseous abnormalities as- study was to provide a detailed guideline of
sociated with shoulder dislocation. the normal MRI developmental anatomy of
2
Department of Radiology, Beth Israel Medical Center, The normal postnatal development of the the proximal humerus in the growing child
New York, NY.
pediatric shoulder has been elucidated on the from infancy through the adolescent years to
3
Department of Radiology, NYU Hospital for Joint basis of cadaveric and radiographic studies skeletal maturity.
Disease, New York, NY. [1, 2]. MRI, however, has a unique advantage
compared with other modalities because it Materials and Methods
AJR 2014; 202:418–425
enables clear visualization of the nonossified Our HIPAA-compliant study was approved by
0361–803X/14/2022–418 cartilaginous epiphysis, the secondary ossifi- the institutional review board of New York Uni-
cation centers, and the physis. Studies using versity Langone Medical Center. The requirement
© American Roentgen Ray Society MRI have examined the general patterns of for informed patient consent was waived. A ret-
rospective search for all MRI examinations of the Other sequences, which were occasionally per- 1). Its shape conformed to the final shape of
shoulder or upper extremity including the shoulder formed, included FLASH (TR/TE, 798/17.9; sec- the humeral head. Preossification centers,
performed at our institution between January 2003 tion thickness, 3 mm; matrix, 256 × 144). When which manifested as small foci of low sig-
and May 2012 in patients under 18 years old was infection or tumors were suspected, the studies nal intensity measuring a few millimeters in
conducted using our digital databank. Exclusion were usually composed of: axial T1-weighted (TR size on T1-weighted images and bright sig-
criteria included inadequate imaging studies, gross- range/TE range, 400–424;/10–11; section thick- nal intensity on fluid-sensitive images, were
ly distorted anatomy, or abnormality in the proximal ness, 3 mm; matrix, 192–256 × 144–192), axial seen in three shoulders in two patients. In
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humerus signified by abnormal signal intensity. and sagittal T1-weighted with fat saturation (TR a 2-month-old patient with bilateral shoul-
Two radiologists (with 25 and 7 years of experi- range/TE range, 423–589/10–11; section thick- der studies, the preossification centers were
ence in musculoskeletal radiology) retrospectively ness, 3 mm; matrix, 192–256 × 134–192) before identified at the expected locations of the
reviewed the MRI studies in consensus. The fol- and after the administration of IV contrast ma- medial humeral head secondary ossification
lowing variables were reviewed: presence, num- terial (gadopentetate dimeglumine, Magnevist, centers. In a 4-month-old patient with an os-
ber, and fusion of secondary ossification centers; Bayer HealthCare), axial T2-weighted with fat sified medial head secondary ossification
appearance and closure of the growth plate; pres- saturation (TR range/TE range, 3590–4000/64– center, the preossification center was found
ence of metaphyseal stripe; and presence of proxi- 70; section thickness, 3 mm; matrix, 192–256 × in the greater tuberosity (Fig. 2).
mal metaphyseal marrow signal intensity. Other 125–179), and coronal T1-weighted (TR range/TE By 4–10 months (n = 7), a single ossifica-
imaging modalities, including radiography and range, 400–423/10–11; section thickness, 3 mm; tion center was apparent in the medial half of
CT, were also reviewed when available. matrix, 192–256 × 163–192). the humeral head in all patients. It was asym-
MRI was performed with either 1.5 T (Mag- metrically positioned and had an oval shape
neton Aera and Avanto, Siemens Healthcare) or Results that did not conform to the cartilaginous
3 T (Magneton Skyra and Magneton Verio, Sie- A total of 105 MRI studies were reviewed shape of the humeral head. Initially, in the
mens Healthcare). There was some variability in in 94 patients, ranging in age from 2 months very young age group, the ossification center
the MRI technique depending on patient age and old to 17 years old. Twenty-two of the 105 was intermediate in signal intensity on both
indication for the study. A head coil was used in studies were excluded for the following rea- T1-weighted and fluid-sensitive images, con-
patients 2–6 months old with the shoulders in the sons: inadequate imaging quality (n = 10) or sistent with red marrow signal intensity (Fig.
center of the coil, a head and neck coil was used significant humeral abnormality, including 2). But in the older infants, the ossification
in patients 12 months to 5 years old, and a shoul- fracture (n = 4), tumor (n = 3), osteomyeli- center showed fatty marrow signal intensity
der surface coil was used in the older patient pop- tis (n = 4), and extensive bony deformity re- on all pulse sequences (Fig. 3).
ulation. The following sequences were performed lated to brachial plexus injury (n = 1). The By 10 months, a second smaller oval-
in most patients: coronal proton density-weight- final patient cohort consisted of 76 patients, shaped ossification center had also formed
ed (TR range/TE range, 2100–2300/30–35; FOV, accounting for 83 MRI studies (32 girls and in the greater tuberosity (Fig. 3B). This os-
12–14 cm; section thickness, 2–3 mm; section 44 boys). Indications for the MRI studies sification center always appeared only after
gap, 1 mm; matrix, 256–320 × 240) or coronal included normal findings (n = 9), pain (n = the formation of the first ossification center
proton density-weighted with fat saturation (TR 16), rule out labral tear (n = 12), rule out ro- in the medial aspect of the humeral head.
range/TE, 2000–2100/36; section thickness, 3 tator cuff pathology (n = 9), brachial plex- Only one 3-year-old patient showed multi-
mm; matrix, 192 × 115–125), coronal T2-weight- us injury (n = 8), soft-tissue tumor (n = 8), ple small ossification centers (Fig. 3C). In all
ed fast spin echo with fat saturation (TR range/ trauma (n =6), dislocation (n = 4), rule out other cases, only two major secondary ossi-
TE range, 2500–4800/54–58; echo train length, acromioclavicular-coracoid pathology (n = fication centers were identified. There was a
7; FOV, 12–14 cm; section thickness, 3 mm; sec- 4), rule out septic arthritis (n = 2), rule out 1-year age gap in the patients sampled from
tion gap, 1 mm; matrix, 320–512 × 230–392), ax- bony tumor (n = 2), decreased range of mo- 2 to 3 years old. As a result, we were unable
ial proton density-weighted (TR range/TE range, tion (n = 1), spina bifida (n = 1), and labral to examine osseous fusion at that age inter-
2420–3890/31–39; section thickness, 3 mm; ma- repair (n = 1). val. However, by 3–5 years (n = 4), the two
trix, 256–512 × 187–208) or axial proton density- The studies were subdivided into the fol- major secondary ossification centers had al-
weighted with fat saturation (TR range/TE range, lowing categories according to patient age: ready started the process of osseous fusion
2700–2900/35–41; echo train length, 7; FOV, 12– 0–4 years old, n = 19 (12 girls, seven boys); (Fig. 3D), beginning anteriorly and progress-
14; section thickness, 3 mm; section gap, 1 mm; 5–9 years old, n = 12 (five girls, seven boys); ing posteriorly.
matrix, 256 × 256), sagittal T1-weighted (TR 10–13 years old, n = 17 (five girls, 12 boys); In the 5- to 9-year-old age group, the two
range/TE range, 500–765/8.4–20.0; FOV, 12–14 and 14–17 years old, n = 35 (13 girls, 22 boys). major secondary ossification centers contin-
cm; section thickness, 3 mm; section gap, 1 mm; ued to expand and further fused together.
matrix, 256–320 × 240–256), and sagittal T2- Humeral Head Ossification As the secondary ossification centers grew,
weighted with fat saturation (TR range/TE range, In the 0–4 years age group, one 3-month- they lost their oval configuration and became
3100–4000/59–80; FOV, 12–14 cm; section thick- old patient did not show evidence of second- more hemispherical, with a flat base against
ness, 3 mm; section gap, 1 mm; matrix, 256–336 × ary ossification centers; all other patients the growth plate and a round superior sur-
224–256). In a few patients, coronal and sagittal had one or more ossification centers. The face, which progressively conformed to the
STIR imaging was performed instead of fluid- nonossified cartilaginous epiphysis was ho- articular surface of the humeral head (Fig.
sensitive sequences (TR range/TE range, 2980– mogeneously intermediate in signal inten- 3D). None of the cases showed a separate
4820/39–75; slice thickness, 1–3 mm; matrix, sity on T1-weighted images and low in sig- lesser tuberosity secondary ossification cen-
192–320 × 144–321; inversion time, 150–170 ms). nal intensity on fluid-sensitive images (Fig. ter. Instead, the larger secondary ossification
Discussion
Our study assessing the progression of
normal development of the proximal humer-
us on MRI concentrated on the secondary
ossification centers, growth plate, metaphy-
seal stripe, and marrow signal-intensity al-
A B terations in the proximal metaphysis. We
noted a sequential pattern of development
that for the most part was similar to the re-
sults of prior cadaveric and radiographic
studies (Fig. 8).
The secondary ossification centers under-
go a sequential change in MRI signal-inten-
sity characteristics, which correlates with
the histologic and structural changes that
take place within the epiphysis. The progres-
sion of events begins with chondrocyte hy-
pertrophy at the site of future secondary os-
sification centers, followed by vascular and
osteoblast invasion from adjacent cartilage
canals and subsequent lysis of the hypertro-
phied cells. At this time, synthesis of bone
C D and formation of the secondary ossification
Fig. 3—Development of secondary ossification centers. centers occur [1, 9, 10]. The MRI signal in-
A, Proton density–weighted coronal image (TR/TE, 2100/36) in 5-month-old boy shows single ossification tensity of the preossification centers, low on
center (arrow), asymmetrically positioned within medial humeral epiphysis and showing fatty marrow signal T1-weighted and bright on fluid-sensitive im-
intensity. Rest of humeral head and greater tuberosity are intermediate in signal intensity, consistent with
nonossified epiphyseal cartilage (asterisk).
ages, likely correlates with the presence of
B, Proton density–weighted coronal image (TR/TE, 2100/36) in 20-month-old boy shows fatty marrow within vascular invasion and lysis of the chondro-
two secondary ossification centers in medial humeral head and greater tuberosity, respectively (arrows). cytes. Once osteoid has been laid down, the
C, Proton density–weighted coronal image (TR/TE, 2160/35) in 3-year-old girl shows at least three secondary humeral head secondary ossification centers
ossification centers (arrows) within humeral head and greater tuberosity. Rest of nonossified humeral head is
intermediate in signal intensity (asterisk). show low to intermediate signal intensity on
D, T1-weighted coronal image (TR/TE, 400/10) in different 3-year-old girl shows early fusion (white arrow) all pulse sequences, consistent with red mar-
between humeral head and greater tuberosity ossification centers. Centers have become more hemispherical, row [11, 12]. At this stage, the secondary
with flat bases (black arrows) against growth plate and round superior surfaces, which conform to articular
surface of humeral head and to greater tuberosity, respectively (arrowheads). ossification centers can be difficult to dis-
tinguish from the adjacent nonossified epiph-
ages 3 and 9 years. In patients older than 15.5 creasing age, the red marrow signal intensity yseal cartilage on T1-weighted and fluid-sen-
years, the presence of the metaphyseal stripe was progressively more concentrated in the sitive sequences. With red to yellow marrow
began to fade and disappear. In these cases, it proximal metaphysis. Occasionally, in the 0- conversion, the secondary ossification cen-
was either minimal (n = 9) or completely ab- to 4-year-old age group (n = 7), the signal ters develop the easily visualized typical fat-
sent (n = 8). Any residual stripe, before com- intensity appeared on fluid-sensitive images ty marrow signal intensity.
pletely disappearing in these older patients, as a linear stripe of bright signal intensity Ogden et al. [1] reported the histologic pres-
was better visualized posteriorly. on the metaphyseal side of the growth plate, ence of humeral head preossification centers,
contributing to its multilaminar appearance. manifested by chondrocyte hypertrophy, cen-
Proximal Metaphyseal Marrow Signal Intensity In the 10- to 13- (n = 13) and 14- to 17-year- tral vascularization, and early osteoid forma-
During the first few months of life, the old (n = 19) age groups, the residual bright tion. To the best of our knowledge, however,
proximal humerus was diffusely low signal signal intensity was either linear or patchy in the MRI signal-intensity characteristics of the
intensity (brighter than adjacent muscle) on appearance (Fig. 7). By 15 years, when the preossification centers in the proximal humer-
T1-weighted images and bright signal inten- growth plate was partially closed, the signal us have not been documented. Preossification
sity on fluid-sensitive images, consistent with intensity manifested more as a linear band centers on MRI in the trochlea have been de-
red marrow signal intensity (Fig. 1). With in- abutting the epiphysis. Around the time of scribed in several studies [4, 13, 14]; these re-
A B C
Fig. 5—Growth plates in proximal humerus.
A, Proton density-weighted fat-suppressed coronal image (TR/TE, 2840/25) in 14-year-old girl shows pyramidal and jagged, multilaminar growth plate (arrowheads). Bright signal
intensity of growth plate is bordered by low-signal-intensity epiphyseal bone plate (white arrow) and metaphyseal zone of provisional calcification (black arrow).
B, Secondary growth plate, depicted as spherical stripe of bright signal intensity (arrows), surrounding greater tuberosity secondary ossification center (asterisk), is
noted on T2-weighted turbo spin-echo fat-suppressed sagittal image (TR/TE, 3800/64) in 20-month-old boy.
C, Closure of growth plate is seen as loss of normal bright signal intensity in physis (arrowheads) on proton density-weighted fat-suppressed coronal image (TR/TE,
3200/45) in 15-year-old girl. Only posterolateral region remains open (arrow).
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