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Fate of osteocytes in adult mouse whole bone isografts and homografts.

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Fate of Osteocytes in Adult Mouse Whole Bone
Isografts and Homografts'
KARL K. NISHIMURA: JAMES A. YAEGER3 AND TAWFIK Y. SABET
Department of Histology, University of Illinois at the Medical Center and
Department o f Orthopedic Surgery, Presbyterian-St. Luke's Hospital,
Chicago, Illinois
It is well established that fresh bone
autografts or isografts are more successful
than homografts (Herndon and Chase,
'54; Curtiss, Chase and Herndon, '56; Anderson, Dingwall, Schmidt, Le Cocq and
Clawson, '61; Sabet, Hidvegi and Ray,
'61b). Autografts and isografts vascularize more completely, show continued
growth and differentiation of young or
embryonic bone with generous new bone
formation, and are rapidly and more completely incorporated within the host (Ray,
Degge, Gloyd and Mooney, '52; Chase and
Herndon, '55; Siffert, '55; Felts, '57; Heslop, Zeiss and Nisbet, '60). In most of
these studies a great proportion of the
cellular elements was found to survive
autotransplantation for a long period of
time. Fresh bone homografts, on the other
hand, evoke an immune host response
(Campbell, Brower, MacFadden, Payne
and Doherty, '53; Bonfiglio, Jeter and
Smith, '55; Chalmers, '59; Sabet et al.,
'61b). This reaction is generally characterized by inferior vascularization of the
recipient site, prolonged cellular reaction
with round cell infiltration, fibrous encapsulation, sporadic and scanty osteogenesis,
and progressive degeneration with final
absorption or rejection of the transplant
(Chalmers, '59; Heslop et al., '60; Anderson, '61; Sabet et al., '61b, '62). Since the
failure of most osteocytes to survive homotransplantation was constantly associated
with the inferior results obtained, one
may conclude that there is a relation between cell survival and the homograft reaction.
One previous comprehensive quantitation of osteocyte survival in bone transplantation has been reported. Although this
work differed from the present study in the
type of animal used, size and preparation
of the bone transplant, age, and method
of transplantation, it represents the only
comparable study of which we are aware.
Heslop et al. ('60) reported on osteocyte
survival, osteogenesis, and the host reaction in a study comparing autologous and
homologous bone transplants. Tibial segments were transplanted subcutaneously
into young adult rats. The surviving osteocytes in a portion of the tubular cortex
were counted and tabulated as a percentage of lacunae counted. They noted a
band of osteocytes near the outer surface of the tubular cortex surviving up
to 250 days in both experimental groups.
The autografts showed a higher proportion of surviving cells than the homografts,
with a significant difference being established by 35 days.
The purpose of the present investigation was to determine the proportion of
osteocytes persisting in the diaphyses of
adult whole bone isografts and homografts. Differences in the survival levels
of the two experimental groups might provide a quantitative index of the effects of
the host-transplant reaction. Also, the
study was designed to investigate the fate
of osteocytes in different locations within
the diaphysis to determine if the reaction
was uniform throughout.
MATERIALS AND METHOD
The third metatarsals of inbred Strong
A mice, six to eight months old, of both
sexes, were used as grafts. They were
1 This investigation was supported by P.H.S. Research Grants A-3220 and A-1339 from. the National
Institutes of Health. From a dissertatlon submitted
by Karl K. Nishimura in partial fulfillment of the
requirements for the M.S. Degree III the Graduate
College, The University of Ilhnois at the Medical
Center.
2 Supported by a Fund for Dental Education Fellow-
shin.
----< 3
U.S.P.H.S. Research Career Development Award
Recipient.
85
86
KARL K. NISHIMURA, JAMES A. YAEGER AND T A W F I K Y. SABET
transplanted subcutaneously into transparent chambers (Sabet, Hidvegi and
Ray, '61a) previously placed in six to
eight month old inbred male mice of
Strong A (as isografts) and CBA (as
homografts) strains. Host animals were
sacrificed at intervals of 10,20, 30,45, and
60 days post-grafting, and the grafts dissected out. A total of 114 specimens were
available for this study. The grafts were
~ e indneutral formalin, decalcified with
EDTA at pH 5.4 and imbedded in celloidin.
Longitudinal serial sections were cut, and
stained with hematoxylin and eosin.
From each specimen, two to six sections
were obtained. Generally, only one sec-
I
I
I
I
PROXIY4L
I
tion extending the entire length of the
diaphysis and representing the mid-longitudinal axis was selected for counting.
Where it was not possible to obtain a well
oriented section, two to three slides of the
same specimen were used for complete
coverage of the diaphysis. The number
of specimens counted is indicated in table
1.
The relative number of persisting osteocytes was determined by counting under
high power (X430) the areas of the diaphysis illustrated in figures l-a and l-b.
Micrometer and Howard discs were used
to demarcate the circumferential strata in
each high power field. Corresponding
CLYTR4L
I
I
I
DISTAL
I
I
I
A
Diaphyssal
Divisions
PROXIMAL
......................P E R I O S T L A L .......................................................................
MID -CORTI C A L
....... .......................................................................................................
MCOULLARY
MARROW
CAVITY
.....................................................................................................................
.....................................................................................................................
B
Circumferential
Strata
Figure 1
a Outline drawing of a longitudinal section of a metatarsal indicating the longitudinal
divisions.
b Square from proximal division of figure 1-a enlarged, indicating circumferential strata.
87
OSTEOCYTES IN BONE TRANSPLANTS
areas on either side of the marrow cavity
were alternated for counting, several
fields being required. The distribution of
cells was not uniform throughout, and in
many instances three to five fields were
necessary to fulfill the quota for the periosteal and medullary strata. Counting was
restricted to the lacunae of the orginal
transplant and excluded those of any new
bone formed after transplantation.
Seventy-five lacunae were counted in
each longitudinal division (proximal, central, and distal), 25 for each circumferential stratum (periosteal, mid-cortical,
and medullary) in a division. The counts
were also tabulated to indicate totals of
75 lacunae for each complete circumferential stratum. Thus, a grand total of
225 cells was counted per specimen. The
data were expressed as a ratio of persisting
osteocytes to the total number of lacunae
counted (75 or 225).
0
I
I
I
10
20
The identification of persisting osteocytes was based on the presence of a purple-staining, intact, plump nuclear mass
within the lacunae. Empty lacunae and
those containing fragmented or obviously
shrunken nuclei were counted as dead
osteocytes.
The great majority of persisting osteocytes exhibited normal morphology with
purple-stained intact nuclei and distinct
nuclear granules. However, it was difficult to distinguish between a normal nucleus and one that had reached the early
stage of pycnosis. Accordingly, moderately
pycnotic nuclei were probably tabulated as
persisting in this study (fig. 5 ) .
RESULTS
The detailed description of the histological and vascular behavior of the grafts
will be the subject of a later publication.
In summary, the onset and pattern of vascularization appeared to be similar for
both groups. Initial vascularization ap-
I
30
I
I
I
40
50
60
Doys
Fig. 2 Osteocytes persisting in whole isografts and homografts. Mean f 1 Standard
Deviation.
88
KARL K. NISHIMURA, JAMES A. YAEGER AND TAWFIK Y. SABET
TABLE 1
Osteocytes p e d s t i n g in entire diaphyses
Ftsf
Number of
specimens
counted
grafting
Experimental
group
10
Isograft
Homograft
7
20
Isograft
Homograft
4
30
Isograft
Homograf t
4
45
Isograft
Homograf t
4
60
Isograft
Homograft
2
0
Control
Persisting osteocytes
per 225 lacunae
mean f 1 std. dev.
168 &16.2
2
161 -C 10.6
0.10
1202 11.3
0.05
98? 19.2
0.02
9 8 2 4.2
0.10
151 k19.9
3
129 k 6.3
5
122 219.6
2
115.5-C 2.1
3
4
peared as early as ten days and continued
to become firmly established in isografts,
but less well established in homografts.
Following an initial inflammatory response,
most of the homografts were encapsulated
by fibrous tissue and were only loosely attached to the connective tissue of the
host. Scanty periosteal and endosteal bone
apposition was noted on the grafts of both
series as early as ten days post-grafting.
New bone overlaid cellular as well as
acellular areas of some transplant. In both
isografts and homografts the original
whole bone transplant remained intact
with little change in gross morphology. In
general, the host immune response was
mild (Sabet et al., ’62).
57 k 18.6
218
P value of
unpaired
“t” test
isograft vs
homograft
* 5.8
0.05
-
tion of the “t” test (unpaired) showed a
significant difference at this time interval
( P = 0.05). In the succeeding periods
both groups showed a progressive diminution in the number of persisting osteocytes,
isografts decreasing less rapidly and remaining relatively constant after 30 days.
By 60 days the percentage of remaining
osteocytes in the isograft series was approximately twice that of the homograft
(51.3% and 25.3%). A comparison of
the means for time intervals of the two
series showed a significant difference ( P =
0.02) of the overall reaction (table 4).
In no instance was an isograft or homograft specimen found to be entirely devoid
of lacunae with stained, intact nuclei.
Persistence of osteocytes in the
Persistence of osteocytes in the
entire diaphysis
longitudinal divisions
Counts of non-transplanted control meCounts of persisting osteocytes showed
tatarsals showed that an average of 96.8% no significant differences between the three
of the lacunae contained normal osteo- longitudinal divisions in either the isocytes. The cells were evenly distributed graft or homograft series (table 2, figs.
throughout the diaphysis.
3-a, 3-b). At ten days the proportion of
In both experimental series, the total osteocytes remaining in all divisions was
number of persisting osteocytes dropped similar for both experimental groups, but
rapidly during the first ten days, both thereafter all the homograft divisions asshowing a loss of approximately 25%
Figure 3
(table I, fig. 2 ) . By the end of 20 days,
a Osteocytes persisting in isograft longituhowever, the isograft series showed a dinal
divisions.
higher proportion of persisting osteocytes
b Osteocytes persisting in homograft longithan did the homograft series. Applica- tudinal divisions.
89
OSTEOCYTES IN BONE TRANSPLANTS
10
r
9(
-
8(
I
a
2.
Y
7c
0
v)
0
sc
m
.
c
..-*
5c
v)
a
0
40
L
0
30
-=
0
0
20
-
-
Proximal
______
Y
L
Central
e
10
Distal
A
0
-
I
I
I
I
I
I
10
20
30
Days
40
50
so
I
so
so
Distal
B
I
I
I
I
10
20
30
Days
40
Figure 3
I
90
KARL K. NISHIMURA, JAMES A. YAEGER AND TAWFIK Y . SABET
TABLE 2
Osteocytes persisting in longitudinal divisions
Persisting osteocytes per 75 lacunae. Mean -I- 1 std. dev.
Days
Homograft
Isograft
Proximal
Proximal
Distal
Central
Central
Distal
10
57
2 7.5
57 2 7.3
55 i. 8.2
5 4 2 4.2
54 2 7 . 1
53 2 7 . 7
20
47
211.3
57
2 2.3
47
42rt11.2
44
34
2 2.9
2a*
f 11.4
39.52~ 2.8
k5.6
26.4
30
46.5)- 6.8
43
35 k a . 0
35 28.9
45
41 f 1 3
42 k 6.3
39
5.7
2 9 5 5.6
34.5*9.2
34.5kQ.7
60
40 212.7
39.5*10.5
36 f 4.2
2 4 k 5.8
13 2 5 . 2
20 k 8 . 5
Control
73 2 2.3
73 2 2.6
72 -t- 1.5
-C
sumed a lower level, reflecting the overall
homograft-isograft difference described
above.
4.5
grafts had only 6% and the isografts 30%
of their original osteocytes persisting in
the medullary stratum.
The proportion of osteocytes persisting
in the periosteal stratum of both series lay
between the mid-cortical and medullary
strata, and this relationship was maintained throughout the observation period.
CeIl dissolution appeared to be most rapid
in the medullary stratum, moderate in the
periosteal, and least in the midcortical.
In this respect the three strata behaved
similarly in isografts and homografts with
the latter assuming a lower level, again
reflecting the overall difference.
A comparison of the means for the time
intervals of the three isograft and homograft circumferential strata showed highly
significant differences between the periosteal and medullary strata but not between
the mid-cortical strata. A summary of the
results including tests of significance on
the related behavior of these three circumferential strata is presented in tables 3
and 4.
Persistence of osteocytes in the
circumferential strata
An unexpected observation was the high
proportion of nucleated lacunae in the midcortical portion of the diaphysis. The persisting osteocytes seemed to predominate
in this deep stratum in both homografts
and isografts by a significant margin over
the periosteal and medullary strata (tables
3 and 4, figs. 4-a, 4-b). The width of this
layer of osteocytes approximated one-third
of the cortex but varied slightly from specimen to specimen and also in different
parts of the same transplant. In the isografts the proportion of osteocytes in this
mid-cortical stratum decreased gradually.
At the end of 60 days, 79% of the osteocytes still remained. The homograft midcortical stratum, as in the isograft, showed
the highest percentage of remaining osteocytes. The decrease was gradual for the
first 20 days, but thereafter cell dissoluDISCUSSION
tion occurred at a more rapid rate dropThe results of this study do not agree
ping to 52% by 60 days.
with previous reports that all cellular eleA second interesting observation was ments are destroyed in cortical bone transthe more rapid and higher mortality found plants (Phemister, '14; Pollock, McKenney
in the medullary stratum than in the peri- and Blaisdell, '29; Reynolds and Oliver,
osteal stratum of both series. The statis'50) nor do they suport the hypothesis
tical signscance of this difference was that all cellular elements survive (Albee,
marginal when individual values were
compared within separate time intervals
Figure 4
(table 3), but the T' values were much
a Osteocytes persisting in isograft circumlower, denoting greater significance, when ferential strata. Mean f 1 Standard Deviation.
mean values for time intervals were comb Osteocytes persisting i n homograft circumpared (table 4). By 60 days the homo- ferential strata. Mean -C 1 Standard Deviation.
91
OSTEOCYTES IN B O N E T R A N S P L A N T S
100 -)
5
2 0 1
Poriorteol
-
Mid- Cor l i c a I
Medullary
A
0
------
_._.-.I
I
I
I
I0
9.0
I
I
30
Days
Figure 4
I
I
40
I
J
I
1
80
a0
92
KARL K. NISHIMURA, JAMES A. YAEGER AND TAWFIK Y. SABET
TABLE 3
Osteocytes persisting in circumferential strata
P value of paired “t” test
Days
Experimental
SOUP
Persisting osteocytes per 75 lacunae
Mean
1 std. dev.
+-
pen!:kal
Midcortical Periosteal
VS.
VS.
medul- medullary
larv
Periosteal
Midcortical
Medullary
czhzH1
46 214.2
41 f 6.3
0.02
0.17
0.004
0.04
0.33
0.20
10
Isograft
Homograft
54 flO.O
54 f 0.1
68 k 2.2
66 k 4.2
20
Isograft
Homograft
49 2 5.3
34 & 8.3
67
7.2
63 2 2.0
35
8.6
22 2 3.2
0.002
0.02
0.001
0.002
0.02
0.15
30
Isograft
Homograft
44.5212.0
34 214.6
62.5f 2.6
52 f 8.5
22
12
4.2
4.9
0.08
0.08
0.001
0.001
0.07
0.03
45
Isograft
Homograft
42 2 3.3
28.52 3.5
56 2 8.3
56 f 0.1
24 f 9.0
13.52 0.7
0.02
0.06
0.002
0.01
0.01
0.09
60
Isograft
Homograft
32 C 7.7
13 2 5.8
59 2 1.4
39 k10.6
24 2 4.2
5
3.6
*
0.17
0.02
0.04
0.02
0.37
0.13
Control
73 2 1.5
72 2 3.3
73 f 1.7
-
-
-
0
*
*
f
*
TABLE 4
Comparison o f combined means in circumferential strata P values f r o m paired
“t” tests between means f o r time intervals
HOMOGRAFT
ISOGRAFT
0.0I
M i d - Cortical
0.11
Mid-Cortical
Total
0.02
Total
’44). They do however, confirm the findings of Chalmers (’59), Heslop et al. (’60)
and Anderson (’61), that a proportion of
osteocytes persist in both isografts and
homografts. In the present study a significant difference between the isografts
and homografts is apparent by 20 days.
0.004
The proportion of persisting osteocytes
shows an apparent quantitative relationship to the adverse host response in the
homografts. Although statistically significant, the difference may not be sufficiently
great to provide an accurate index of a
milder homograft reaction. Therefore, the
OSTEOCYTES IN BONE TRANSPLANTS
93
94
KARL K. N I S H I M U R A , JAMES A. YAEGER AND TAWFIK Y. SABET
usefulness of "relative osteocyte persistence" as a method for testing measures enhancing the acceptance of homografts is
limited.
The question of viability or non-viability
of osteocytes persisting in cortical bone
transplants has received attention in recent literature (Ray, La Violette, Buckley
and Mosiman, '55; Kiehn and Gutentag,
'57; Anderson et al., '61). An empty
lacuna is an indication that the osteocyte
has died and disappeared. However, the
routine histological criterion for establishing viability, i.e., the presence of morphologically normal, purple staining nuclei, is
now disputed as sufficient evidence of
cell survival. Harris and Ham ('56), Anderson ('61) and Ham and Leeson ('61)
asserted that cells deep in cortical bone
were non-viable after transplantation regardless of the presence of stainable material. They reasoned that the canalicular
mechanism of cortical bone was so inefficient that deeper cells could not possibly
survive transplantation after being severed
from their normal blood supply and environment. Osteocytes may appear to be
living as long as they are surrounded by
intact bony matrix which protects them
from lysis by the host. Therefore, the
presence of stained, intact nuclear material in a lacuna may not necessarily indicate viability of the osteocyte.
Heslop et al. ('60) and Chalmers ('59)
on the other hand, also observed histologically that osteocytes persisted in cortical
bone transplants but suggested that these
osteocytes occupied a protected position
similar to the interior of a diffusion chamber. The cortical bone could be a barrier
to host cells but permit fluid exchange.
Abbot, Schottstaedt, Saunders and Bost
('47) reported that cells of a bone graft
could survive up to 15 days, without a
demonstrable blood supply, in the fluids
of the host bed. By the intracellular uptake of a radioactive isotope (P39, Kiehn
and Gutentag ('57), further demonstrated
the viability and survival of osteocytes in
homografted bone that was kept in a millipore diffusion chamber for four months.
Evidence seems to support the possibility
of viable osteocytes persisting in cortical
bone under proper conditions.
No essential differences in morphological or staining characteristics of persisting
nuclei between isografts and homografts
and normal bone were apparent in this
study. Normally staining, intact nuclei
containing granules were observed in the
lacunae of 60 day homografts (fig. 5 ) and
isografts. The supposition that an osteocyte dies without showing degenerative
nuclear changes within 60 days does not
seem plausible. It is doubtful whether
viability or non-viability can be established
with certainty using routine hematoxylineosin staining and light microscopy. However, this does not detract from accepting
the morphologic evidence as indicating
relative, rather than absolute, values of
osteocyte survival.
In the present study no significant differences were apparent in the proportion
of osteocytes persisting between the diaphyseal divisions (figs. 3-a, 3-b). This is
not surprising in view of the morphology
of the mouse metatarsal. The tubular cortex is fairly uniform in thickness, diameter and structure throughout the diaphysis (fig. l-a) unlike other long bones
such as the femur and tibia.
The behavior of the three circumferential strata is of interest since the pattern is similar in both isografts and homografts. Osteocyte persistence is greatest
in the mid-cortical stratum, moderate in
the periosteal, and least in the medullary.
The periosteal circumferential stratum
comes into immediate and direct contact
with the tissue fluids of the host bed. This
surface presumably would be accessible to
both host tissue fluids and inflammatory
cells, favoring the death and dissolution
of some osteocytes, but allowing the survival of those not destroyed by the host.
The medullary circumferential stratum
occupies a unique position because the
transplants were whole bones, in which the
marrow cavity is isolated from the host
environment until vascularization occurs.
Therefore, there is a lag period (ten days)
before re-establishment of circulation to
the marrow cavity. During this interval
the osteocytes closest to the medullary surface must compete with the myeloid elements for materials in the stagnant fluids
of the marrow cavity. Due to the limited
OSTEOCYTES IN BONE TRANSPLANTS
access of these fluids to the osteocytes, most
die and eventually disappear.
The mid-cortical circumferential stratum, on the other hand, is farthest from
either periosteal or medullary environment (70-80 p for the deepest cells) and
yet, apparently, it is the least affected.
This portion of the cortical diaphysis has
the highest proportion of nucleated lacunae
in both isografts and homografts. The
reason for the persistence of these osteocytes is unknown. Assuming they are living, they must depend on diffusion from
either the periosteal or medullary surfaces
for obtaining nutrients and removal of
waste products, but they are protected
from destruction by the barrier of matrix
surrounding them.
The fate of osteocytes i n freshly transplanted bone depends on a multiplicity of
factors interacting with a cumulative effect to produce a favorable or unfavorable
environment. Since there is no clear understanding of the physiology of transplanted bone, a n explanation of osteocyte
persistence based on granulation tissue
formation, circulatory, and immunological
factors is necessarily inconclusive. However, the consistency of the present observations suggests a predictable pattern
of osteocyte response to bone transplantation, the response of the cells depending
on their positions within the bone and
the nature of the transplant.
SUMMARY
Metatarsals from adult Strong A (isografts) and CBA (homografts) mice were
transplanted into subcutaneous sites in
Strong A hosts using a transparent chamber technique. After intervals of 10, 20,
30, 45 and 60 days the 114 transplants
were dissected free and longitudinal sections prepared. The proportion of intact
nuclei in 75 lacunae was counted in each
of three longitudinal diaphyseal divisions
(proximal, central and distal) and three
circumferential strata (periosteal, midcortical and medullary).
Nuclei persisted u p to 60 days in both
isografts (51.3% of lacunae nucleated)
and homografts 25.3% ). A significantly
higher proportion of osteocytes was found
to -persist in isografts than- homografts as
95
early as 20 days after transplantation
(67.1% vs. 53.3%, P = 0.05). No significant differences were found among the
longitudinal divisions in either isografts
or homografts. As early as ten days after
transplantation, osteocyte persistence in
the mid-cortical circumferential stratum
was greatest and that in the medullary
stratum least in both isografts and homografts. These differences persisted to 60
days ( P s at 60 days, 0.01-0.001).
Osteocyte persistence depended upon the
position of the cells within the bone. Cells
in the mid-cortical stratum were best protected from the host immune reaction,
while cells in the medullary stratum apparently had a n inadequate tissue fluid
exchange until the transplants were vascularized.
ACKNOWLEDGMENT
We are indebted to Dr. Robert D. Ray
for his encouragement and for the courtesy
of his laboratory facilities and staff i n the
preparation of this material.
LITERATURE CITED
Abbot, L. C., E. R. Schottstaedt, J. B. deC. M.
Saunders and F. C. Bost 1947 The evaluation of cortical and cancellous bone as grafting material. A clinical and experimental
study. J. Bone Jt. Surg., 29A: 3 8 1 4 1 4 .
Albee, F. H. 1944 Evolution of bone graft
surgery. Am. J. Surg., 63: 421-436.
Anderson, K. J. 1961 The behavior of autogenous and homogenous bone transplants in
the anterior chamber of the rat’s eye. J. Bone
Jt. Surg., 43A: 980-995.
Anderson, K. J., J. A. Dingwall, J. Schmidt, J. F.
LeCocq and D. K. Clawson 1961 The effect
of particle size of the heterogenous bone transplant on the host tissue. 11. A histological
study. Ibid., 43A: 996-1004.
Bonfiglo, M., W. S . Jeter and C. L. Smith 1955
Immune reactions in tissue homotransplants.
Ann N. Y. Acad. Sci., 59: 4 1 7 4 3 2 .
Campbell, C. J., T. Brower, D. G. MacFadden,
E. B. Payne and J. Doherty 1953 Experimental study of the fate of bone grafts. J.
Bone Jt. Surg., 35A: 332-346.
Chalmers, J. 1959 Transplantation immunity
in bone homografting. Ibid., 41B: 160-179.
Chase, S. W., and C. H. Herndon 1955 The fate
of autogenous and homogenous bone grafts.
A historical review. Ibid., 37A: 809-841.
Curtiss, P. H., Jr., S. W. Chase and C. H. Herndon
1956 Immunological factors in homogenous
bone transplantation. 11. Histological studies.
Ibid., 38A: 324-330.
Felts, W . J. L. 1957 A comparison of subcutaneous implants of isolog&s and homolo-
96
KARL K. NISHIMURA, JAMES A. YAEGER AND TAWFIK Y . SABET
gous immature whole mouse bones. Transplant.
Bull., 4: 131-135.
Ham, A. W., and T. S. Leeson 1961 Histology,
4th Edition. J. B. Lippincott Co., Philadelphia,
pp. 334-338.
Harris, W. R., and A. W. Ham 1956 The
mechanism of nutrition i n bone and how it
affects its structure, repair and fate on transplantation - In Ciba Symposium on Bone
Structure and Metabolism (Ed. by G. E. W.
Wolstenholme). Little, Brown and Co., Boston,
pp. 135-143.
Herndon, C. H., and S. W. Chase 1954 The
fate of massive autogenous and homogenous
bone grafts including articular surfaces. Surg.
Gyn. Obst., 98: 273-290.
Heslop, B. F., I. M. Zeiss and N. W. Nisbet 1960
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adults, whole, osteocyte, isografts, homograft, mouse, bones, fate
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