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Periosteal appositional bone growth from age two to age seventy in man. A tetracycline evaluation

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Periosteal Appositional Bone Growth from Age Two to
Age Seventy in Man
A TETRACYCLINE EVALUATION '
BRUCE N. EPKER2 AND HAROLD M. FROST3
Orthopedic Research Lnboratory, Henry Ford Hospital,
Detroit, Michigan
ABSTRACT
Periosteal appositional bone formation in human ribs was analyzed.
Tetracycline labels deposited in uiuo reveal that in human ribs there can be continued
apposition of periosteal bone after age 20, which decreases in amount with advancing
age but is still present in the seventh decade.
It has been tacitly assumed that periosteal osteoblastic activity and the concomitant periosteal apposition of new bone,
which cause an increase in the outside
diameter of a bone during its growth and
development, ceases at or shortly after
skeletal maturity, which occurs at about
age 20 (Todd, '37; Krogman, '62; Tonna
and Cronkite, '62). This concept has recently been challenged on the bases of
studies of human ribs and femurs, in
which increases in transverse dimensions
were found to continue well past age 40
(Trotter et al., '60; Sedlin et al., '63; Smith
and Walker, '64). It would be desirable
to confirm these findings by some means
which provides unequivocal and direct evidence that periosteal bone apposition does
indeed continue after skeletal maturity,
since this would (i) remove any doubt that
sampling errors were present in these
studies, and (ii) prove that periosteal bone
formation remains active throughout life.
Over 400 mineralized, complete crosssections of the middle third of the fifth,
sixth or seventh rib from 92 metabolically
normal individuals were studied (Frost,
'58). The age ranged from 2 to 70 years,
and the bones had been labeled in viuo on
one or more occasions with a tetracycline
antibiotic, which was usually given to treat
infections. These ribs were selected for
study on the bases that: (i) examination
of mineralized cross sections with the fluorescence microscope showed one or more
tetracycline labels to be present somewhere
in the bone, showing that a tetracycline
antibiotic had been given at some time
prior to skeletal sampling, and (ii) the
ANAT. REC.,154: 573-578.
TABLE 1
T h e fourth column expresses as n per cent the
fraction of the labeled subjects that hnd a circumferential lamellar (see footnote 6 , p . 5 7 5 ) tetracycline label. However, the size (i.e., circumference) o f labels i n older people was much less than
i n children, so the per cent figures do not indicute
absolute differencesi n the amount o f labeled bone,
Age group
Total number individuals
Number of
of labeled
with a
individuals
periosteal
label
0-9
10-19
12
5
11
20-29
30-39
40-49
50-59
60-69
20
20
13
7
15
14
12
4
2
5
92
52
Totals
4
P$gzt
pe;',"b"a'
92
80
70
60
31
29
33
Mean56.4
individual was known to have had no
serious metabolic disease or intrinsic bone
disease prior to sampling. About three
quarters of these cases were sampled at
autopsy at the county medical examiner's
office, causes of death including suicide,
homicide, trauma, drowning and exposure.
The remainder of the cases supplied rib at
thoracotomy for nondebilitating lesions
such as hiatus hernia, lung and mediastinal biopsy and repair of patent d u c t ~ s . ~
1 Work supported b
rants AM-04186 of National
Institutes of HeaJth, et esda, Md., and Project 293,
Henrv Ford HosDital.
2 Rksident, Department of Oral Surgery, Henry Ford
Hospital, ,Detroit 2, Michigan.
3 Associate
Orthopaedic Surgeon Department of
Orthopaedic Surgery, Henry Ford Hbspital, Detroit 2,
Michigan.
4 We are deeply indebted to the generosity of E. S.
Zawadski, M.D. for the autopsy material and to R.
Tabor, M.D., C. Lam, M.D. and T. Gehagen, M.D. for
material obtained at thoracotomy.
3%
573
574
BRUCE N. EPKER AN D HAROLD M. FROST
As reported in 1957 by Milch, Rall and
Tobie, any of the tetracycline group of
antibiotics will produce a permanent label
or tissue marker at each place in the skeleton where new bone formation was active
while the antibiotic was being administered
(Milch et al., '57) see figure 1. In 44 of
these cases the antibiotic was given at
times known to us, and they proved to have
been labeled an average of 46 months prior
to sampling, the range being 0.1 to 10.5
years. While in the remaining 48 cases
this information was not available, it is
reasonable to assume that approximately
similar figures apply to them.
The 400 rib sections were studied by
fluorescence microscopy to detect tetracycline labels in the subperiosteal circumferential lamellae, and when one or more
such labels were present the fact was re-
Fig. 1 The light bands are labels of tetracycline antibiotics as they appear under
fluorescence microscopy. This is a rib cross-section from a nine-year-old child who had four
separate labels incorporated in the cutaneous periosteal circumferential lamellae as it was
drifting (to the right) during growth. Periosteum to the right, marrow cavity to the left
( 8 x ) . The bright, wavy line crossing the marrow space in the lower half :is a cotton fiber
embedded in the mountant.
PERIOSTEAL BONE GROWTH
575
Fig. 2 Rib cross-section (166 x ) from a 37-year-old female. The India ink markers separate
two tetracycline labels incorporated in the periosteal circumferential lamellae.
corded. Therefore, while all of the cases
in this study had some tetracycline labeled
bone, not all of them had labels deposited
in the subperiosteal circumferential lamellae.5*6The data are shown in table 1.
RESULTS
Ninety-two per cent of the children
under age ten who had received tetracycline had a label in the subperiosteal
lamellae, usually on the cutaneous cortex
(see fig. 1). With increasing age, there
was a significant decline in the per cent of
labeled people who had periosteal labels,
the level being 33% in the seventh decade.
We also observed that the size (i.e., circumference), of labels in older people was
much less than in children, so the figures
in table 1 do not indicate absolute differences in the amount of labeled bone between young and old (see figs. 2, 3).
DISCUSSION
It has generally been assumed that after
skeletal maturation periosteal osteogenic
activity was active only in pathological
states or/and in fracture healing, i.e., that
after skeletal maturity bones do not get
bigger. In this regard, it has been suggested that with increasing age bone cells
respond with less vigor (Tonna and Cronkite, '62). But recent studies of periosteal
remodeling, bone surface drift, and of age
related changes in bone mass, volume and
cross-sectional area, have suggested that
the periosteal bone surface remains active
and in positive bone balance (i.e., in sum,
continually adds bone so that the periosteal
envelope continues to enlarge) throughout
life (Trotter et al., '60; Sedlin et al., '63;
Smith and Walker, '64; Epker and Frost,
'65). If this were so, tetracycline labels
should be incorporated into periosteal circumferential lamellae in adults as well as
in children. This study shows that this is
the case.
5 Labeled: had been given a tetracycline antibiotic.
Label: tetracycline that had been deposited in newly
forming bone.
6 Circumferential lamellae are the layers of new
lamellar bone deposited immediately under the penosteum. This specifically excludes Haversian systems,
and thus any tetracycline labels i n Haversian systems.
576
BRUCE N . EPKER A N D HAROLD M. FROST
Fig. 3 Rib Cross section (166 X ) from 66-year-old male. The light band to the right is a tetracycline label incorporated i n the periosteal circumferential lamellae.
We found that: (i) new periosteal bone
apposition occurs throughout life, and (ii)
with increasing age, a decreasing fraction
of the labeled cases revealed circumferential lamellar labeling. The rapidly growing
child, as compared to the adult, demonstrates significantly more sites of new
periosteal bone apposition. However, even
those persons aged 60 to 70 show some
evidence of such appositional growth.
At no age were 100% of the periosteal
surfaces labeled. This could mean one of
two things: (i) periosteal bone formation is
normally intermittent, so that at some
moment a label will not be deposited; (ii)
or periosteal bone formation had stopped
permanently in those individuals who
lacked a periosteal label. It is unreasonable to assume that (ii) is true in children,
which implies that (i) is the correct interpret ation.
Most of the labels at all ages had been
covered over by 5 to 30 CI of new unlabeled
periosteal circumferential lamellae bone
(see figs. 2, 3 ) . This must have been added
after the time of labeling but before skeletal sampling. Since Auneomycin, the first
tetracyline antibiotic was first marketed
in 1950, there can be no doubt that all
labeled patients older than age 35 received
their label after skeletal maturity.
These findings are coiiclusive evidence
that human periosteal bone apposition can
continue after skeletal m,aturity.
LITERATURE CITED
Epker, B. N., and H. M. Frost 1965 A histological study of remodeling at the periosteal,
haversian canal, cortical endosteal, and trabecular endosteal surfaces in human ribs. Anat.
Rec., 152: 129-136.
Frost, H. M. 1958 Preparation of thin, undecalcified bone sections by rapid manual
method. Stain Technol., 33: 272-276.
Krogman, W. M. 1962 The Human Skeleton in
Forensic Medicine. Charle's C Thomas, Springfield, Ill., p. 227.
Milch, R. A ,, D. P. Rall and J. E. Tobie 1957
Bone localization of the tetracyclines. J. Nat.
Cancer Inst., 19: 87-93.
PERIOSTEAL BONE GROWTH
Sedlin, E. D., A. R. Villanueva and H. M. Frost
1963 Variations in cross section area of rib
cortex with bone. Gerontology, 18: 9-13.
Smith, R., and R. Walker 1964 Femoral expansion i n aging women: implications for osteoporosis and fractors. Science, 145: 156-157.
Todd, T. W. 1937 Atlas of Skeletal Maturation (Hand). Mosby, St. Louis.
577
Tonna, E. A., and E. P. Cronkite 1962 Changes
in the skeletal cell proliferative response to
trauma concomitant with aging. J. Bone and
Joint Surg., 44A: 1557-1568.
Trotter, M., G. E. Broman and R. R. Peterson
1960 Densities of bones of white and negro
skeletons. J. Bone and Joint Surg., 42A: 50-58.
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periosteum, seventh, two, growth, evaluation, tetracyclic, apposition, age, man, bones
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