Download as pdf or txt
Download as pdf or txt
You are on page 1of 8

Pe d i a t r i c I m a g i n g • O r i g i n a l R e s e a r c h

Kwong et al.
MRI of Proximal Humerus in Children

Pediatric Imaging
Original Research

Skeletal Development of the


Downloaded from ajronline.org by 110.137.72.198 on 01/18/24 from IP address 110.137.72.198. Copyright ARRS. For personal use only; all rights reserved

Proximal Humerus in the Pediatric


Population: MRI Features
Steven Kwong1 OBJECTIVE. The purpose of this study was to provide a guideline of normal MRI devel-
Shefali Kothary 2 opmental anatomy of the proximal humerus in a growing child.
Leonardo Lobo Poncinelli 3 MATERIALS AND METHODS. Retrospective interpretation of 83 consecutive MRI
studies of shoulders in children 2 months to 17 years old was performed in consensus by two
Kwong S, Kothary S, Poncinelli LL radiologists. The following variables were documented: presence, number, and fusion of sec-
ondary ossification centers; appearance and closure of the growth plate; presence of the me-
taphyseal stripe; and proximal metaphyseal marrow signal intensity.
RESULTS. Preossification centers were seen in 2- and 4-month-old patients. Secondary
ossification centers appeared in the medial humeral head and greater tuberosity at 4 and 10
months, respectively, originally depicting red marrow and later converting to yellow marrow.
A separate lesser tuberosity ossification center was not seen. The ossification centers began
fusing by 3 years and gradually conformed to the final shape of the proximal humerus. Ossifi-
cation was completed by 13 years. The multilaminar growth plate initially had a flat and smooth
contour that progressively became irregular and pyramidal, closing at 17 years. The metaphy-
seal stripe was noted at infancy and disappeared by 15.5 years. The metaphyseal marrow signal
intensity was diffusely low in infants but, with conversion to yellow marrow, showed proximal
metaphyseal bright patchy or linear signal-intensity, eventually disappearing by 17 years.
CONCLUSION. The postnatal skeletal development of the proximal humerus in the pe-
diatric population follows distinctive sequential patterns of maturation, which can serve as a
guideline for interpreting MRI studies in children.

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-

418 AJR:202, February 2014


MRI of Proximal Humerus in Children

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
Downloaded from ajronline.org by 110.137.72.198 on 01/18/24 from IP address 110.137.72.198. Copyright ARRS. For personal use only; all rights reserved

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

AJR:202, February 2014 419


Kwong et al.

Fig. 1—Cartilaginous tour. The apex of the plate pointed superior-


humeral head with nearly
flat growth plate and
ly and moved from a relatively central posi-
low diffuse proximal tion in the anterior humeral head to a much
humeral marrow signal more lateral position posteriorly. The coni-
intensity in 2-month- cal appearance of the growth plate persist-
old boy. STIR coronal
image (TR/TE, 4820/75) ed throughout skeletal immaturity (Fig.
shows homogeneous 5A). Starting within the 5- to 9-year-old age
Downloaded from ajronline.org by 110.137.72.198 on 01/18/24 from IP address 110.137.72.198. Copyright ARRS. For personal use only; all rights reserved

intermediate signal group, the margins of the growth plate were


intensity consistent
with nonossified
no longer smooth but depicted a more ragged
cartilage in humeral head and irregular appearance (Fig. 5A).
(asterisk). Note slightly The growth plate showed cartilage MRI
arched growth plate signal-intensity characteristics with interme-
(arrowheads). There
is also homogeneous diate signal intensity on T1-weighted images
intermediate signal and increased signal intensity on fluid-sensi-
intensity in proximal tive images. A multilaminar appearance was
humeral diametaphysis
consistent with red seen with increased patient age on the fluid-
marrow (stars). sensitive images; the normal physeal bright
signal intensity was bordered by a linear
margin of low signal intensity on its epiphy-
seal side, consistent with a bony plate and by
a less-well-defined low-signal-intensity zone
of provisional calcification on its metaphyse-
al side (Fig. 5A). The growth plate measured
a few millimeters in size and was of equal
thickness throughout its course. A ringlike
stripe of bright signal intensity surrounding
the medial head and greater tuberosity ossifi-
cation centers was occasionally seen, compat-
ible with the secondary growth plate (Fig. 5B).
In all but two cases, the growth plate re-
mained completely open until 14 years. The
two exceptions showed partial closure at 9
years. At times, it was difficult to assess the
growth plate closure due to its marked modula-
tion and secondary partial volume averaging.
A B
Leading up to 14 years, the pattern of clo-
Fig. 2—Preossification center in greater tuberosity and secondary ossification center, depicting red marrow in sure began with gradual narrowing and de-
medial humeral head in 4-month-old girl. creasing signal intensity of the growth plate.
A and B, Preossification center (white arrow) is low in signal intensity on T1-weighted (TR/TE, 603/11) (A) From 14 to 16 years (n = 19), the growth plate
and bright in signal intensity on T2-weighted fat-suppressed (TR/TE, 3470/101) (B) axial images, suggesting
fluid collection. Medial head secondary ossification center (black arrow) is low in signal intensity on both showed partial closure. The posterolateral re-
sequences, compatible with red marrow. Lymphatic malformation (asterisk, B) is incidentally seen. gion of the growth plate was the last area
to close (Fig. 5C). By 17 years (n = 8), the
center in the medial humeral head extended insertion of the subscapularis tendon, which growth plate had completely closed in all but
anteriorly into the nonossified lesser tuberos- conformed to the final shape of the lesser tu- two patients.
ity (Fig. 4A). berosity (Fig. 4B). In two cases, a 13-year-
The older age groups showed further old patient and a 15-year-old patient, we were Metaphyseal Stripe
growth of the humeral head secondary ossi- unable to determine whether the lesser tuber- For patients between 5 months and 1 year
fication centers. By 13 years old and older, osity ossification was complete. old, in more than half of the studies (four of
most cases showed complete ossification of six cases) the proximal humeral metaphysis
the proximal humerus (n = 5 in the 10- to Growth Plate showed a circumferential thin stripe of in-
13-year-old age group, n = 26 in the 14- to In the first few months of life, the proxi- termediate signal intensity on T1-weighted
17-year-old age group). In two cases, com- mal humeral growth plate was relatively flat images and bright signal intensity on fluid-
plete ossification was noted as early as 11 and transversely oriented, with a slight cen- sensitive images, which paralleled and sep-
years old. The lesser tuberosity was the last tral upward arch (Fig. 1). During this period, arated the humeral cortex from the adja-
portion of the proximal humerus to fully os- the margins of the growth plate were rela- cent low-signal-intensity periosteum (Figs.
sify, showing in most studies a persistent in- tively smooth. Beginning at about 4 months, 3D, 5A, and 6). This metaphyseal stripe was
termediate-signal-intensity, crescentic, sliver the growth plate progressively transformed noted in babies a few months old up to the
of cartilaginous anlage deep in relation to the into a tented or conical (pyramidal) con- 14-year-old patients, except for two patients,

420 AJR:202, February 2014


MRI of Proximal Humerus in Children

growth plate closure at about 17 years, the


signal intensity was either imperceptible or
completely absent. In six cases, we were un-
able to adequately assess the proximal me-
taphyseal marrow signal intensity because
the fluid-sensitive sequences were either sub-
optimal or not performed.
Downloaded from ajronline.org by 110.137.72.198 on 01/18/24 from IP address 110.137.72.198. Copyright ARRS. For personal use only; all rights reserved

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-

AJR:202, February 2014 421


Kwong et al.

graphically evident until 3 years. The time


frame of the study by Ogden et al. was more
comparable to the findings in our study, in
which the earliest medial head and greater tu-
berosity ossification centers appeared on MRI
at 4 months and 10 months, respectively. Our
data also show the process of osseous fusion
Downloaded from ajronline.org by 110.137.72.198 on 01/18/24 from IP address 110.137.72.198. Copyright ARRS. For personal use only; all rights reserved

starting at 3 years beginning anteriorly and


progressing posteriorly, again in agreement
with the observations of Ogden et al.
The appearance of a third ossification cen-
ter in the lesser tuberosity continues to be a
topic of debate. Some sources suggest that a
third ossification center may occur in the less-
er tuberosity at 5 years, fusing with the other
A B two ossification centers at 6–7 years [16, 17].
Fig. 4—Maturation of lesser tuberosity. Clarke et al. [8], in an MRI study of the prox-
A, Gradient-echo FLASH axial image (TR/TE, 798/17) in 22-month-old boy shows medial head secondary imal humerus, showed an image with a dis-
ossification center (white arrow) extending anteriorly into nonossified lesser tuberosity (black arrow). Second tinct lesser tuberosity ossification center. On
greater tuberosity ossification center is also seen (arrowhead).
the other hand, Ogden et al. [1], on the basis
B, Fat-suppressed proton density-weighted axial image (TR/TE, 3030/33) in 12-year-old patient shows
intermediate signal intensity in lesser tuberosity (arrow), consistent with nonossified cartilage. of histologic and radiologic studies, did not
mention a third ossification center. Scheuer
port similar MRI signal-intensity characteris- in the humeral head is noted in a small per- and Black [18] questioned the existence of
tics to the preossification centers identified in centage of white newborns. Caffey [2] stat- a separate lesser tuberosity ossification cen-
our shoulder studies, with low signal intensity ed that the humeral head ossification center ter and argued that even if one does exist, it
on T1-weighted images and bright signal in- is radiographically present as early as with- is only for a short time. Our study, in agree-
tensity on fluid-sensitive images. The preossi- in the first month of life and that the greater ment with that of Ogden et al., did not show a
fication centers with their fluid signal-intensity tuberosity ossification center appears by 4–5 separate lesser tuberosity ossification center in
characteristics should not be mistaken for an months. Ogden et al. [1], on the other hand, any of the patients. Instead, the larger ossifica-
intraepiphyseal abscess. Other findings associ- reported that the first ossification center in tion center in the medial humeral epiphysis ex-
ated with infection, such as abnormal soft-tis- the humeral head is evident on radiographs panded anteriorly into the lesser tuberosity in
sue, cartilage, and marrow signal intensity and by 2–3 months and that the greater tuberos- all of our patients. It is conceivable, however,
periosteal reaction should aid in distinguishing ity ossification center appears by 7 months. that a small lesser tuberosity ossification cen-
an abscess from a preossification center. Ogden et al. further stated that although, his- ter was present in some of our patients but had
Kuhns et al. [15] reported, based on chest tologically, osseous fusion beginning anteri- already fused with the medial humeral head
radiography, that the first ossification center orly commences at 2 years, it is not radio- ossification at the time of imaging. Interest-

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).

422 AJR:202, February 2014


MRI of Proximal Humerus in Children

tilaminar signal-intensity characteristic of


the proximal humeral growth plate is similar
to that of other joints [3]. It is hypothesized
that the central bright signal intensity of the
femoral physeal cartilage, composed of hy-
aline, includes the germinal and prolifera-
tive zones and part of the hypertrophic zone.
Downloaded from ajronline.org by 110.137.72.198 on 01/18/24 from IP address 110.137.72.198. Copyright ARRS. For personal use only; all rights reserved

This signal intensity is brighter than that of


the surrounding hyaline cartilage because of
increased cellularity and a greater amount of
free water in the physis relative to the rest of
the epiphysis.
Initially, the proximal humeral phy-
sis showed smooth margins and was mild-
ly arched. With growth, the borders of the
A B physis became more irregular. A gradual
Fig. 6—Metaphyseal stripe in proximal humerus. change from a flat to a conical tented ap-
A, T2-weighted axial image (TR/TE, 2100/60) in 20-month-old boy shows circumferential thin bright signal pearance of the plate was also seen, compat-
intensity (white arrow) separating humeral cortex (black arrow) from adjacent low-signal-intensity linear ible with prior reports [1, 2, 7]. The growth
periosteum (arrowheads).
B, Stripe (arrow), best seen on medial side of humeral metaphysis, is also noted in proton density–weighted plate remained open until about 14 years, al-
coronal image (TR/TE, 2500/28) in 9-year-old girl. though partial closure was noted in two pa-
tients, both 9 years old. Gradual thinning of
the plate and eventual closure, manifested
by loss of the bright signal intensity, were
noted by about 17 years, confirming previ-
ous skeletal studies [19]. The posterolateral
aspect of the growth plate was the last re-
gion to disappear. This was compatible with
the prior reports by Ogden et al. [1], who
stated that the closure of the growth plate
begins centrally.
We noted a circumferential metaphyseal
stripe in the proximal humerus in the large
majority of our skeletally immature patients
from a few months of age up to 14 years.
This manifested as linear bright signal in-
Fig. 7—Increased tensity on fluid-sensitive images, which par-
metaphyseal marrow
signal intensity in 15-year- alleled and was interposed between the low-
old boy. T2-weighted signal-intensity proximal diametaphyseal
coronal image (TR/TE, cortex and the low-signal-intensity perios-
3500/72) shows patchy
teum. As the patients reached skeletal ma-
bright signal intensity
in proximal metaphysis turity around the time of growth plate clo-
(asterisk). Metaphyseal sure, the possibility of seeing the stripe
stripe is also visualized was markedly decreased. The metaphyseal
(arrow).
stripe in the proximal humerus is likely the
ingly, our study showed that the lesser tuber- The growth plate showed typical multi- equivalent of the stripe noted on MRI along
osity remained incompletely ossified until the laminar signal-intensity characteristics on the posterior surface of the distal femoral
adolescent years, in one patient as late as 15 fluid-sensitive sequences. This consisted of and proximal tibial metaphyses [20]. Sim-
years. This manifested in the older children central bright signal intensity of the physeal ilar to our results, Laor et al. [20] found a
as a sliver of cartilage signal intensity deep cartilage, bordered superiorly by linear low statistically significant correlation between
in relation to the insertion of the subscapular- signal intensity of the epiphyseal bony plate the presence of the stripe at the knee and
is tendon. To the best of our knowledge, the and by a less well-defined low signal intensi- skeletal immaturity (patency of the growth
late ossification of the lesser tuberosity has ty depicting the zone of provisional calcifica- plate). Furthermore, histology depicted the
not been previously reported and may be of tion on the metaphyseal side [3]. The proxi- stripe to represent a highly vascularized fi-
diagnostic importance because cartilaginous mal metaphyseal region occasionally had brous tissue deep in relation to the loosely
bright signal intensity should not be misinter- linear increased signal intensity approximat- attached periosteum, which was hypothe-
preted as a partial insertional tear of the sub- ing the plate, further contributing to the mul- sized to be related to intramembranous bony
scapularis tendon. tilaminar appearance of the region. The mul- growth. Recognizing this stripe as a normal

AJR:202, February 2014 423


Kwong et al.

Fig. 8—Drawing shows mal developmental changes from disease in


developmental stages
of proximal humerus by
the skeletally immature patient.
age. First humeral head
secondary ossification Acknowledgment
center appears in We sincerely thank Zehava Sadka Rosenberg
early infancy in medial
humeral head, followed for the original idea for this work and her
by additional secondary constant instruction throughout the research.
Downloaded from ajronline.org by 110.137.72.198 on 01/18/24 from IP address 110.137.72.198. Copyright ARRS. For personal use only; all rights reserved

ossification center in We are grateful for the countless hours she


greater tuberosity. Fusion
of ossification centers
spent reading MRI studies, revising this ar-
begins at 2–3 years ticle, and mentoring us throughout the proj-
and is complete by late ect. We all agree that this study would not
puberty. Growth plate have been possible without her supervision
metamorphoses from
gentle arc at infancy into and support.
pyramidal appearance in
early years to full closure References
by late adolescence.
Metaphyseal stripe 1. Ogden JA, Conlogue GJ, Jensen J. Radiology of
(arrow) disappears at postnatal skeletal development: the proximal
about time of growth plate humerus. Skeletal Radiol 1978; 2:153–160
closure. Gray indicates
2. Caffey J. Pediatric x-ray diagnosis, 8th ed. Chi-
nonossified epiphyseal
cartilage, and white cago, IL: Year Book Medical Publishers,
circles indicate secondary 1972:434–437
ossification centers. 3. Laor T, Jaramillo D. MR Imaging insights into
skeletal maturation: what is normal? Radiology
MRI finding in the proximal humerus as gesting pathologic marrow edema, such as 2009; 250:28–38
elsewhere is important to avoid mistaking it that which is seen in Little League shoulder. 4. Jaramillo D, Waters PM. MR Imaging of the
for periosteal elevation related to pathologic Comparison of the signal intensity with that normal developmental anatomy of the elbow.
processes, such as tumor, osteomyelitis, or of adjacent muscle can aid in distinguishing Magn Reson Imaging Clin N Am 1997; 5:501–
fracture. The latter disease entities are typi- the two entities. In Little League shoulder, 513
cally associated with extensive marrow and the T1-weighted low signal intensity is typi- 5. Chung T, Jaramillo D. Normal maturing distal
soft-tissue edema. Osseous destruction and cally lower than that of adjacent muscle. Fur- tibia and fibula: changes with age at MR imag-
soft-tissue masses in tumors, Brodie abscess thermore, asymmetry and stress-related ir- ing. Radiology 1995; 194:227–232
in osteomyelitis, and cortical disruption in regularities in the growth plate will also be 6. Zawin JK, Jaramillo D. Conversion of bone
fractures can further aid in distinguishing the present [21]. In comparison, in healthy chil- marrow in the humerus, sternum, and clavicle:
normal metaphyseal stripe from true disease. dren, the red marrow T1-weighted signal in- changes with age on MR images. Radiology
Zawin and Jaramillo [6] reported that bone tensity is higher than adjacent muscle, and 1993; 188:159–164
marrow in the humerus as elsewhere begins the growth plate is relatively smooth with 7. Chauvin NA, Jaimes C, Laor T, Jaramillo D.
initially as red marrow, which as early as equally thick margins. Magnetic resonance imaging of the pediatric
1–5 years converts to yellow marrow in an Aside from the small sample size, the shoulder. Magn Reson Imaging Clin N Am 2012;
orderly, sequential manner. The conversion most significant limitation of our study is 20:327–347
first occurs in the proximal epiphysis, central the small number of healthy cases (n = 9) in 8. Clarke SE, Chafetz RS, Kozin SH. Ossification
diaphysis, and distal metaphysis and, in pa- our patient cohort. These studies were usu- of the proximal humerus in children with resid-
tients 15 years old and older, terminates in ally included in the FOV for comparison, ual brachial plexus birth palsy: a magnetic reso-
the proximal metaphysis [6]. This pattern is particularly in the younger patient popula- nance imaging study. J Pediatr Orthop 2010;
consistent with our findings, in which in in- tion. The retrospective nature of our study 30:60–66
fants the marrow signal intensity in the prox- and lack of histologic and surgical confirma- 9. Gray DJ, Gardner E. The prenatal development
imal humerus was diffusely low in signal in- tions are other limitations. Many of our MRI of the human humerus. Am J Anat 1969;
tensity on T1-weighted sequences (higher studies lacked gradient-echo images, which 124:431–445
than adjacent muscle) and bright in signal may have been more optimal for assessing 10. Shapiro F, Holtrop ME, Glimcher MJ. Organi-
intensity on fluid-sensitive images, suggest- the secondary ossification centers. zation and cellular biology of the perichondrial
ing that the entire humerus was composed In summary, our study provides an MRI ossification groove of Ranvier. J Bone Joint
of red marrow. With skeletal growth, the red guide to the normal skeletal maturation of Surg Am 1977; 59:703–723
marrow signal intensity became increasing- the proximal humerus in the pediatric popu- 11. Jaramillo D, Laor T, Hoffer FA, et al. Epiphy-
ly concentrated in the proximal metaphysis lation. This guide, which covers the appear- seal marrow in infancy: MR imaging. Radiolo-
and eventually disappeared around 17 years, ance of the humeral head secondary ossifi- gy 1991; 180:809–812
comparable to the timeline in the study by cation centers, growth plate transformation, 12. Taccone A, Oddone M, Dell’Acqua A, Occhi M,
Zawin and Jaramillo. At times, the increased metaphyseal stripe, and proximal metaphy- Ciccone MA. MRI “road-map” of normal age-
proximal metaphyseal marrow signal inten- seal marrow signal intensity, will hopefully related bone marrow. Pediatr Radiol 1995;
sity in our patients was quite striking, sug- provide a road map for differentiating nor- 25:596–606

424 AJR:202, February 2014


MRI of Proximal Humerus in Children

13. Jaimes C, Jimenez M, Marin D, Ho-Fung V, Ja- 16. Cocchi U. Zur frage der epiphysenossifikation Epiphyseal union at the upper limb and scapular
ramillo D. The trochlear pre-ossification center: des humeruskopfes das tuberculum minus. Ra- girdle in a modern Portuguese skeletal sample.
a normal developmental stage and potential pit- diol Clin 1950; 19:18–23 Am J Phys Anthropol 2008; 137:97–105
fall on MR images. Pediatr Radiol 2012; 17. Rockwood CA, Matsen FA. The shoulder, 4th 20. Laor T, Chun GF, Dardzinski BJ, Bean JA,
42:1364–1371 ed. Philadelphia, PA: Saunders/Elsevier, Witte DP. Posterior distal femoral and proximal
14. Chapman VM, Nimkin K, Jaramillo D. The pre- 2009:12 tibial metaphyseal stripes at MR imaging in
ossification center: normal CT and MRI find- 18. Scheuer L, Black S. The upper limb. In: Scheuer children and young adults. Radiology 2002;
Downloaded from ajronline.org by 110.137.72.198 on 01/18/24 from IP address 110.137.72.198. Copyright ARRS. For personal use only; all rights reserved

ings in the trochlea. Skeletal Radiol 2004; L, Black S. Developmental juvenile osteology. 224:669–674
33:725–727 San Diego, CA: Academic Press, 2000:278– 21. Obembe OO, Gaskin CM, Taffoni MJ, Ander-
15. Kuhns LR, Sherman MP, Poznanski AK, et al. 285 son MW. Little leaguer’s shoulder (proximal
Humeral-head and coracoid ossification in the 19. Cardoso HF. Age estimation of adolescent and humerus epiphysiolysis): MRI findings in four
newborn. Radiology 1973; 107:145–149 young adult male and female skeletons. II. boys. Pediatr Radiol 2007; 37:885–889

F O R YO U R I N F O R M AT I O N
The AJR has made getting the articles you really want really easy with an online tool, Really Simple
Syndication, available at www.ajronline.org. It’s simple. Click the RSS button located in the
menu on the right side of the page. You’ll be on your way to syndicating your AJR content in no time.

AJR:202, February 2014 425

You might also like