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Metamorphosis of the joints of the sternum in relation to age changes in other bones.

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Dicision of Physical Anthropology, C. S . National Museiivi
Through his work on the pnbic symphysis, Todd (’20)
established the concept that “certaiii bone areas adjacent to
joints show definite sequence of modification strictly associated with age” (p. 287). Speaking of the symphysis specifically, he stated that “from the eighteenth year onward, the
changes undergone by the pubis are largely if not entirely a
metaniorphosis aiid not an actual growth” (p. 325). Unfortunately, however, he did not pursue this subject much beyond
the s p p h y s i s . at least as regards the lafc-maturing joints of
the postcranial skeleton. Indeed, his summary of the possibilities of finding skeletal age markers, which appears in the
introduction to his study of the symphysis (’20, pp. 287-288),
indicates that he regarded similar studies of certain other
joints, aiid especially those of the sternum, as rather unpromising. P a r t of this statement is worth quoting, nerertl~eless,
because it summarizes joint mctamorpliosis in a masterly way :
I n the main this group [of joints yielding a sequence of modification associated with age] consists of amphiarthroses, namely
the syniphysis pubis, the intercentral joints of the vertebral
column, and the manubrio-gladiolar articulation. But to these
must also be added the sterno-clavicnlar, sa cro-iliac a n d possibly
the eosto-chondral and chondro-sternal joints. The plane between the bone and the articular cartilage of these joints displays features resembling in some degree those of the diaphysoepiphysial plane, and it is upon this fact that the age changes
resolve themselves. Adjacent to these joints “articular” epiph519
incoiiipletely. ci*riitic~iiIly
or iiot ; i t all. Of tlie series
the sterno-clt~\.icnlar area rarly reiiioves itself from consideration throng11 the firsion of tlir c1piphysih at the strrnal twtl of the
clavirle with the slinft of the. bone, while the iiiannbrio-gladiolar
articulation is so chrratic a s apparently t o \\-arrant no confidence.
The intercentral joiiits of the rertebriil coliimn, and tlie pelvic.
tirticulation areas, on tlie other. liantl, a r e niost important. E v ~ n
after tlie last stragglers niriong the epiphyses. namely those of
the spines tincl transverse ~)i*ocesses
of tlie vertebrae, the heads of
the ribs, arid the sternal end of the clavicle, have lost their identity through fiision, tlie line of iinion of the central epiphyses
shows distinct intlepcndenve froin tlie rertebral body. And when
the second of these also tit last, in the early thirties, fails t o register the individi~al’sage. the syniphysis pnbis still retains its
role of time marker. Tndeecl, the syniphysis tells its tale tlironphout life, altliongh Icss clearly from forty years onward than a t
a n earlier age.
?-ses ossify
I d o not bcliclve tliat Todd intended these rcniarks to discourage others from doing reseiirch along the same lines on the
joints of the sternum; I think he was only justifying his o~l’ii
wurse of action by i.eportiiig a wiclel~-hel~cl
belief which he had
not bothered to check adequately. After all, he may have been
well awarc tliat back ill 1890 Thomas Dwight, Professor of
Anatoniy at Harvaid, had expressed the opinion that “the
stciwum is of little raliie a s ail index of age” (p. 532). T l ~ fact
remains, however, that today, a quarter of a century after Todd
studied the pubic syniphpsis, we still cannot read with any
confidence the s i p s of ageing displayed in tlie joints of the
sternum. Also, the need has existed all this time for other
criteria by wliich to assess the aqi of skeletons which have
damaged or missing pelves.
Further accounting for the long-stmiding neglect of age
changes in the strrnum is iIniiccessai’y liere. T will say simply
that ~vlienrecently I ~ v a soffered the opportunity to observe
(at a future date) age cliaiiges in skeletoiis of fully identified
yonng adult males, I decided to csteiid my observations to the
unstudied joints rneiitioned by Todd in tlic ahore quotation.
This clecisioii nccessitatecl a11 exaniinatioii of tlie features ill
question so a s to determine what is significniit f o r iwording
purposes. Having a t liaiicl oiily skeletoiis froni archcological
sources, I could evaluate the observed sequence of hone modification in each joint area only in terms of k n o w i age changes
in other parts of the same skeletons, particularly tooth eruption, cpipliyseal union, sj-mphyseal metamorphosis arid suture
closure. Sirice st17dy of the sternum has proved to be surprisingly rewarding, and since all ohsei*vations of this nature are
useful in skeletal identifications, I feel that my findings on this
bone are worth reporting in advance of the opportunity f o r
smuring more exact dating. (See acldendnrn, p. 528.)
The sternum is uiiique in the number aiid types of its articulations. In addition to tlic mannbriogladiolar or superior intersternal joint, which in most cases is a synchondrosis (fig.
l),‘there are a pair of stcrnoclavicular joints (type: diarthrosis), and usually 7 pairs of chondrosternal joints (types :
first pair a r c syncliondroses ; all others diarthroses). The inferior intersternal joint, that between the corpus of the steriium and the xiphoid process, may be ignored for present purposes. This makes a total of 17 joint areas the metamorphosis
of which may be expected to provide age markers. I n this
coiiiiectioii it is noteworthy that on each side the joints for the
clavicle and first rib, which differ in type (see above), are contiguous, whereas the joint f o r the second rib is located a t the
junction of the inanuhrium and corpus and hence in close relationship with the superior intersternal joint (again 2 joints of
different type i n juxtaposition). Such relationships require
that these two joint complexes be considered as units from the
standpoint of niodification with age. In addition, since the
superior elements of the corpus may not fuse until early in the
third decade, and the joint for the third r i l ~is located a t the
* Gray’s :iliatomy cites Rivitigton siid Maisoiineuve as authorities f o r thc stntonient thiit this joint is diarthrodial in one-third or more of adults, being formed in
these eases perhaps by absorption from the original sprhondrodinl (ampliiarthrodial) form.
line of union, the metamorphosis of the third chondrosternal
joint probably reflects the local rate of ossification.
Todd was correct in stating (see above quotation) that “The
plane between the bone and the articular cartilage of these
joints displays features resembling in some degree those of the
diaphyso-epiphyseul plane ; and it is upon this fact that the age
__ Costo-claviculnr
Fig. 1 Diagrani of tlie upper riid of tlie steriinni showing the different types of
joints. Note that in the case of the first rill (but iiot tlie second or others) bone is
joined to bone by cartilage, without the intervention of a joint earity. Apparently
the sanir is true in most caws for the superior iutcrsternal joint, although the
diagram i s not clear on this point. (After Cuniiinglinni’s fig. 300).
changes resolve themselves.” So f a r as I can discover, all
textbooks of aiiatomy fail to mention epiphyses in descriptions of the ossification of the sternum. Probably this is
due to the delicacy a i d prompt union of the epipliyseal plates
in the areas of the steriial joints. Naturally, unuriited plates
would be lost in skeletal mslccration and hence would not
be seen. On the other hand, the possibility exists that these
plates sometinics are reduced i l l size o r not formed at all, and
this view is supported by such findings a t the stel-nal end of the
clavicle (Todd and d’Errico, ’28).
Although the foregoing anatomical details help explain the
changes observable in the sternum, anyone attempting to
assess age from this bone should first study a series of irnmature specimens in order to appreciate the range of variation
in size, shape and details of joint arrangement. Trainiag the
eye to distinguish between random variation and progressive
modification is essential to correct interpretation of age. I n
the description of the modification sequence that follows, a few
typical specimens have been selected from the many examined
to tell the story. Here, then, variability must be referred to as
something to be taken into account, and not singl!.lcd out for
special treatment.
First, let us look a t a few sterna from in front and arranged
according to physiological growth stages (plate 1). Note that
in only two of the 6 bones displayed is the corpus united into a
single piece of bone. I n the two that are thus united the epiphyses of the long bones a r e also united, and hence these individuals may be regarded a s being past the age of 20 years.
The other 4 bones, being from younger individuals, show various stages of fusion involving different numbers of elements
(between 3 and 5 ) . Also, it is clear that, although the elements
of the corpus a r c erratic in uniting, the top element is generally
the last to fuse. On this basis alone it is often possible to distinguish skeletons of the second and third decades.
Plate 1 also affords a front view of the superior intersternal joint. I n the three examples shown in plate 1, note that the
contact between the manubrium and corpus widens with age.
On this basis one would expect a corresponding progressive
modification of the joint surfaces. Indeed, it is a general rule
for such joints, as Todd was always careful to point out, that
before adulthood the surfaces and borders are rounded and
soft-textured ;but during the third decade angularity and hardtexture appear. Other than this reference to conformity of the
joint surfaces I will not h a r e much to say about the changes in
tlie superioio interstel-nal joint, the reason being that most of
these changes parallel others which deserve more atteiition.
We turn nest to the conjoined articular areas for the clavicle
and first rib at the snperolatcral angle of the manubrium,
Plate 2 sliows 9 manubiia standing 011 edge so as to show the
areas of particular interest and also arranged by physiological
growth stages. Beginning at the left end of the upper row, note
that in the first t h e e the facets for tho clavich and first rib are
poorly differentiated. If 01-eover, the articular surfaces a r e
dimpled or billowcd and h a r e tl matte-like finish or texture.
As will be recognized by those familiar with the skeletons of
a8clolescents,such an appetirancc is typical of a joint in the
stage preceding epiplipseal union. So far as I can judge iio~v
this stage continues here until 17 or 18 years of age.
Before leaving these three specimens, I call attention to tlic
lower edge of the articular area for the first rib. This edge is
well clcfiiiecl in the second rind third specimens but not in the
first. The distinction here is not due to age, hut represents
instclad a comnioii variation. The first specimen is a n example
of a bone in d i c h a t this age all of the borders, except that in
tlie midline superiorly (the jugular iiotch), hare tlie appearance of developing into articular surfaces. I n such a case the
facet for the first rib ultimately would develop a lower edge,
but otherwise the lateral border of the bone would a l w a p reflect the appearance seen here. An unclei-standing of this coiidition makes the pictiire less confusing.
N o w we turn to tlie next three bones in plate 2, that is, the
last two on the top row aiid the first on the bottom row. These
three specimens sliow different stages of epiphyseal union. I n
the first of the t h i w , the epiphysis for the claviculai- facet is
in the process of uniting. There is no iiiclication of an epiplipsis
f o r the adjacent rib facet. Indeed, the latter surface still has
the appearaiice of being prepared to receive a n epiphpsis. Ry
contrast the seconcl specimen has iiicomplctely attached epiphp e a l plates on both surfaces, a i d on the surfaces of the coiijoined intei*stei~naland sccond choiidrosternal joints R S well.
The t1iii.d spccinieii, on the other hand, has progressed still further. Here the articular surfaces a r e completely glazed over.
Yet the appearance of tlie facet f o r the first rib in this third
specimen would suggrst that ail epiphysis for this area never
formed and that a glaziiig of mature bone had served as a
substitute. The latter process is probably of comnion occurrence a,t this site. I n any case, siiice at least two of tlie skeletons iiivolwd a r e in the stage where tlie proximal epiplij-sis of
the humerus is uniting, I would judge that the stage of sternal
maturation under consideration takes place around 19-20 years
of age, although it may extcnd over a longer period.
Before leaving the second group of three bones, I call attention to the developing enlinelice a t about the midpoint in the
conjoined articular areas. As will be seen by looking ahcad in
plate 2, this eminence is to develop into a sharp transverse
ridge which will form tlie boundary between the two welldefined facets. Thus in due course a ridge will provide the
superior edge of the facet for the first rib and the lateral edge
of the facet for the clavicle. However, at the time these articular areas receive their epiphyses, or glaze over, the eminence is still rounded and incompl& ventrally. Until the vcvtral interarticular notch is filled in and the eminence is transformed iiito a transverse ridge delimiting the facets, the
inanubrium cannot be said to have reached maturity. According to present indications the interarticular notch disappears,
and the transverse ridge is formed, when the epiphyses of the
iiiiiominate a1.c about united; in other words, early in the first
half of the third decade.
With these events in mind, we are ready to examine more
closely the last three bones in plate 2. Thc first shows the signs
of maturity just described. I n this case the epiphpsis at the
stcriial end of the clavicle is uniting, which would lie before
25 pears of age according to Todd and d’Errico ( ’28). The
sccoiid differs from the first mainly in haring formed a raised
rim around the edges of the facets for the first and second
ribs. J u s t when the rim appears is not certain, but probably
it is hetween 23 and 30 years of age. Later, as the third speci-
men shows, this rim 8disappcars into the bonv spurs so characteristic of hypertrophic or degenerative arthritis. Between
these eveiits tlie surface of the facet for the first rib becomes
more porous, owing perhaps to the fact thai it is not an arthrodial joint like its neighbors. I am iriclined to believe that this
unique chondrosternal joint is among the first to show degenerative changes. I n any case, arthritic lipping p r o h ~ b l yappears here early in the fourth decade.
We come now to plate 3 showing, with one exception in
lateral view, both the nianubriurn and corpus from 4 individuals. The purpose of this plate is to show two things: (1)
p a r t of the sequence of modificatioii ill the lower chondrosteriial joints, and ( 2 ) vtii*iationin thickness of the superior intersternal joint. The first specimen on tlie left is in the late stage
of maturation already described where, in the manubriuin, the
ventral interarticular notch is just disappearing. Indeed, in
this case the filling-in of tlic notch seems to he taking place
along with the union of cyiphyses in most of the chondrosternal facets. This probably represents one of the sequential
vitriatiotis that one w ~ ~expect
l d to encounter in a large series.
A t least this specimen mikes it clear that all of the chondrosternal facets may have more o r less complete cpiphpseal
plates present tind uniting either just before the ventral
interarticular notch fills in or along with the filling in thereof.
Reference was made in connection with the anatomy of the
joints to the fact that the tliird costal facet may show sigiis of
tlie recent fusion of the upper elements of the corpus. Although
the first specimen in plate 3 scarcely demonstratcs this fact,
the second and third specimens show a division of the third
facet by a transverse cleft. The resemblance in the latter
specimens of the third costal facet and the second costal facet
(as divided by the superior intersternal joint) should be apparent. Observe, however, that the cleft in the third facet is
being bridged over both dorsally and ventrally. The bridges
probably a r e equivalent to the rims of the other joints. Althougli the cleft may persist into middle age, the presence and
thickness of the bridges give some idea of the relative age.
The fourth specimen shows the appearance of the lower costal
facets around middle age and before they develop arthritic
Finally, I call attention to the increased veiitrodorsal thickness of the superior intersternal joints in the second and
fourth specimens. Actually, in the second specimen this joint
is partly fused. As for the fourth specinicn, the manubrium
has been turned so a s to expose the inferior joint surface and
to show that this surface has begun to break down. The appearance suggests that here, too, is an intersternal joint on its
m-ay to fusion. Although thickening of the bone does not always
accompany fusion of this joint, it seems to represent bone reaction connected with joint disturbance, and hence one of the
conditions leading to fusion. Regardless of the causes of
synostosis in this joint, age is not a factor in the process, as
Trotter (’34) has pointed out.
I n view of the need for inforniation about age changes in
the human steriiuiii, I h a r e explored the subject in a series of
skeletons representing the native peoples of North America.
Although, under the circumstances, it is impossible as yet to
assign definite ages to developmental events, and variability in
rate of development cannot be evaluated, the association of
these events with datable age changes in other bones should
prove useful in assessing the age of skeletons. Thus the metamorphosis of the sternal joints in very tentative terms may be
outliiied as follows :
I . C p t o the t i m e t h e proximal epiphysis of the Iiurnerzis
is tmdi”iLg ( u p to 17’-18? y m r s ) .
Component elements of the corpus sterni a r e still identifiable, although those in the inferior two-thirds may have fused.
Joint surfaces here mid in the maiiubrium arc rounded, dimpled or billowed, and exhibit a matte-like surface texture.
2. Coincidelit with, m i d somewhat f o l l o u k g , the u%ioion. of
the proximil epiphysis of the huinwrts (about 19-20B years).
Epiphyscal plates can Iw found in all staaes of uiiioii on the
clavicular facets. At tbc ciid of this period epiphyseal plates
a r e begiiinirig to unite on the rib facets, or failing thc formation of plates, tlie articular snifaces are begiiiiiing to glaze
over. Also, in most cases, tlie superior eleriient of the corpus
is fusing with the clement liest below.
3. CoiiicidmLt zcitk t h c 1 ~ w i o r jof tlic. cyipliyses for the iliac
c r c s t (aid ischiirl rnirius (cihozrt 20-2.7P y w r s ) .
The eminelice marking the boundary between the articular
areas of the clavicle arid first rih gives way to a sharp transTerse ridge. The last step in tlic formation of this ridge is the
filling-in of a ventral interarticular notch. At this time the
facets for the third ribs a r usually
dividccl by a transverse
cleft, the last remaining s i p of the recent fusion of the superior element of the corpns.
4. C'oir~cidc~nt
with crntl iui incilintcly f o l l o w i q irniorb o f the
o p i p h y s i s o t t h o stcriirrl (,nil of tltc rlni;irl~ fabozit 2.?-30?
?Jf flT S ) .
Raised rim is formed around the articular areas of the first
and second ribs arid those of tlie superior intersternal joint.
By this time tlic snpcrior intersternal joint has broadened so
that the articular surfaces arc rectangular. Facets for first
ribs become slightly more poiwis. ('lcfts in facets for third
ribs a r e being bridged across ventrally and dorsally.
5. ,Jirst bcJfore o r coiwirleat with t h e n p p c a r n w c of crrthritis
in f h c 1.ertobrtrc. (cibout 3 5 yfcrrs).
Hypertrophic bone spurs appear around the niargiiis of the
facets for the first ribs, particularly ventrally and dorsally
and nioi-e ahove tliaii below. The othc~r.rib facets develop spurs
much more slom-ly. Also, there may be progressive, disorderly
break-down of the joint surfaces.
A 1) r
) mi ) n r
Whrii this paper was sitbiiiitted f o r publication iii May, 1954, the
opportimitg to piirsne thc subject further seemed unlikely to come
about f o r some time. Yet (.rents took a sndden change by the latter
part of the siiiiiiiier a n d I was able to go t o J a p a n in September for
the purpose of examining the skeletal reinaiiis of American soldiers
recei\7ecl in exchange from the C‘oiunlunists through Operation Glory.
Accordingly, I hare reviewed and corrected the present paper in the
light of this experience. Evtwtually I hope to amplify arid docuiiieiit
the sequence of sternal niotiifications associated with age here merely
(”., AND E. B. JAMIESON(ecls.) 1937 C~uiiiiiiigliam’s Text-Rook of
Anatomy. 7th ed., Oxford Unir. Press, New York.
DWIGHT,THONAS 1890 Tho steruuni as an index of sex, lieiglit and age. .J.
Anat. nud Physiol., 2 4 ; 5“-535.
H. (eil.) 1930 (:lay’s Anatomy of the IIuinnu Body. 231d ed.,
Len and Febiger, Phila.
TODD,T. WINGATE 1920 Age changes in the pubic bone. I. The male white
pubis. A m J . Phys. Anthrop., I I I : 285-334.
J R . 1928 The c1arirul:rr epipliyes. Aui. J .
Anat., 4 1 ; 25-50.
MILDRED1934 Inridenee of synostosis between niauubriuin and body of
the sternuni in Whites and Kegroes. Am. J . Phys. huthrop., X V Z Z I ;
43 9-442.
3 i i 92 3
h’ncicil groicp
murk( r
Ikgiilining union of di&I eliipliysis of Iiunicrus
I’roxiui:il u1ii:ir epipliysis in :id\ awed stage of i i i i i i i i i
Iiegiiiiting uiiioii of proximal epipliysis of humerus
T’rosimal epiphysis of huinerus uniting
Epiphysis at stcriial end of clavicle utiitiug
1,ong bone cpipliyses uniitctl; w r y slight :irtliritis; proI):ild.v Iieginiiitig suture rlosiire
Frout view of a series of sterna selected to diow rertaiu dcre1opmcllt:tl fcaturcs cliscusscd in tlie text. Left to 1iglit:
Top row :
Racial group
s ting
l’rositiid epipligsis of l ~ i i u i c r i ~uui
I.:pipli;vsis for sternal ond of clavicle uuitiiig
Long b o w e ~ ~ i p l i ~ united;
110 arthritis; sottie siiturc clorure
Epipliyses united ; moderate arthritis; adriiiiced suture rlosure
Pcrmauent R1’ erulitctl; distal cyiplipis of liuitic~rusutiiuiitrtl
Beginniug union of distal epiphpis of liunierns
Epiphgsis f o r iiirdial epicoiirlylc of Iiiiiiirriis uuitiiig
Brgiiiiiiiig uuioii of prorinial epipliysis of Iiuuicriis
(No associated holies)
Pliysiologicul age ?iiurk.rr
Lateral yiew of a series of niauubria selected to show eertaiii developutental features diwusscd in the test. From left to
riglit :
Racial group
Epiphysis a t sternal end of clavicle uniting
Epiphysis at sternal end of clavicle united ; no arthritis
Epiphpses united; bcginning arthritis; aclvancc*d suture closure
Beginning arthritis; advanced suture closure
P h p o l o g i c a l age ~ n a r l r r
Lateral view of 4 sterna (1 nisnubrium turned over to show the inferior articular surface) selected to show certain developnieiital features discussed in the text. S o t e the thickening of the bone a t the superior intersternal joint in two of the cases.
From left to right:
GENETICEFFECTOF TRRADIATION.-- There is another basic difference
between irradiating Drosophila eggs and the ovaries of nonpregnant
women, namely, in the reproductive cycles. The Drosophila reproduces
itself in about 10 days. some 30 generations being produced within
one year, although its life cycle is about 90 days. Aftcr irradiation,
little time is left between generations for full recovery from its effects
to take place. In contraht to secondary effects on progeny of the
Drosophila, an interval of at least 20 years elapses between generations
in populations of western countries. Twenty-seven years passed before
a follow-up note could be made on the second “seed generation” in
the case reported here. Thc grandchild appears to be normal by all
pediatric standards.
This is the 5th such casc rccorderl ; Raplan has encountered 4 others.
The long span of tiiiie between generations obviously makes it difficult
to give an absolute answer to the theoretical question of the ultimate
harmful genetic efyect of irradiation on the human race. l h t the long
interval of time between births of a firqt and second generation would
11-arrant the assimption that whatt!ver harmful effects may have been
produced by the x-ray irradiation to the ovaries of a grandmother
would have been dissipated over the years. No acquired let,hal effects
on the genes have becw obserred in hundreds of babies born following
this treatment for the relief of infertility and delayed menstruation.
The additional reeord of 5 normal grandchildren fails to snpport
the claim that low close s-ray irradiation to the ovaries and pituitary
produces harmfnl (ffects in human reproduction.- I. C. Rubin.
Third generation follou-up in xi-onian receiving pelvic irradiation.
J. Am. Med. Assn., vol. 1.50, no. 3, Sept. 20, 1952, pp. 207-209.
KURTB R 6 s T E . - After a long, and as it turned out, hopeless illness,
Kurt Broste, M.D., died in Clopenhagen on the 26th of April, 1954,
at the age of 52. Since 1941 he had been director of the Laboratory
of Physical Anthropology of the 1Jniversity of Copenhagen. Under
his leadership a series of scientific articles were issued from this
institution, articles mainly dealing with the anthropology of prehistoric peoples in Scandinavia as well as in the Eskimo areas. ljnfortunately he did not live long enough to finish his IifeiTorlr, a great
book on “Prehistoric N a n in Denmark” of which only the first volume
has gone into print.
We who are left to continue his work will do our best to keep up
to his brilliant example, always remembering with gratitude his keen
brain, his never failing eheerfnl encouragement and genuine interest
in his pupils.- J . Balsle\- JorFensen, M.D.
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metamorphosis, relations, sternum, change, joint, age, bones
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