Morphologie (2008) 92, 162—170

GENERAL REVIEW

Trabecular bone microarchitecture: A review

La microarchitecture de l’os trabéculaire :
une revue
D. Chappard ∗, M.-F. Baslé , E. Legrand , M. Audran

Inserm, U922, LHEA, Faculty of Medicine, 1, rue Haute-de-Reculée, 49045 Angers cedex, France

Available online 18 November 2008

KEYWORDS Summary The bone mass is constituted during the life by the modeling and remodeling mecha-
Trabecular bone; nisms. Trabecular bone consists in a network of trabeculae (plates and rods) whose distribution is
Microarchitecture; highly anisotropic: trabeculae are disposed parallel to the resultant of stress lines (Wolff’s law).
Histomorphometry; Trabecular microarchitecture appears conditioned by mechanical strains, which are exerted on
MicroCT; the bones of the skeleton. However, few methods are currently clinically validated to appreci-
Remodeling ate and follow the evolution of microarchitecture in bone diseases. The most developed studies
relate to microarchitectural measurements obtained by bone histomorphometry with the use
of new algorithms, which can appreciate 2D various characteristics of the trabeculae, such as
thickness and connectivity. Several works have shown that microarchitecture parameters should
be obtained by using several independent techniques. X-ray microtomography (microCT), micro-
RMI, synchrotron also allow the measurement in 3D of the trabecular microarchitecture in a
nondestructive way on bone specimens. This review describes the evolution of our knowledge on
bone microarchitecture, its role in bone diseases, such as osteoporosis and the various methods
of histological evaluation in 2D and 3D.
© 2008 Elsevier Masson SAS. All rights reserved.

Résumé Le capital osseux se constitue au cours de la vie par les mécanismes de modelage
MOTS CLÉS et de remodelage. Le tissu trabéculaire est constitué par un ensemble de travées (plaques
Os trabéculaire ; et piliers), dont la répartition est hautement anisotrope : les travées se disposent parallèle-
Microarchitecture ; ment à la résultante des lignes de contraintes (loi de Wolff). La microarchitecture trabéculaire
Histomorphométrie ; apparaît conditionnée par les contraintes mécaniques qui s’exercent sur les pièces squelet-
Microtomographie ; tiques. Cependant, peu de méthodes sont actuellement validées cliniquement pour apprécier
Remodelage et suivre l’évolution de la microarchitecture dans les ostéopathies. Les études les plus dévelop-
pées portent sur l’appréciation microarchitecturale par histomorphométrie osseuse grâce à
l’utilisation de nouveaux algorithmes permettant d’apprécier en 2D différentes caractéris-
tiques trabéculaires, dont la connectivité. Plusieurs travaux ont montré que l’appréciation de
la microarchitecture devait utiliser plusieurs techniques indépendantes. La microtomographie X
(microCT), la micro-IRM, le synchrotron permettent aussi de mesurer en 3D l’architecture

∗ Corresponding author.
E-mail address: [email protected] (D. Chappard).
1286-0115/$ – see front matter © 2008 Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.morpho.2008.10.003
Trabecular bone microarchitecture: A review 163

trabéculaire de façon non destructive sur des prélèvements osseux. Cette revue décrit
l’évolution des connaissances sur la microarchitecture osseuse, son rôle dans les maladies
osseuses, comme l’ostéoporose et les différentes méthodes d’évaluation histologique en 2D
et en 3D.
© 2008 Elsevier Masson SAS. All rights reserved.

Introduction mity in all directions). In adults, a preferential orientation

of the trabecular plates is observed along the direction of
Bone, as a connective tissue, is in constant adaptation during the strains, which are exerted on the bone. It is noticeable
all stages of life and two fundamental processes control the that until the 1980s, bone microarchitecture was not taken
bone mass. into account in the comprehension of the pathophysiolog-
Modeling allows the acquisition of the form and the ical mechanisms of metabolic bone diseases; osteoporosis
mass of bone during childhood and adolescence. It ensures was only considered as a disease associated with a reduc-
the growth of the skeletal pieces in length. The osteoblas- tion in the bone mass. At the present time, definition
tic activity is prevalent on the osteoclastic activity (and of the osteoporosis, according to the WHO and Interna-
can occur even in the absence of a resorption step). tional Osteoporosis Fundation (IOF), is ‘‘a systemic skeletal
The modeling activity occurs in the primary spongiosa, disease characterized by low-bone mass and microarchi-
under the growth plates when spicules of calcified carti- tectural deterioration of bone tissue, leading to enhanced
lage are covered with bone. In membranous bones (such bone fragility and a consequent increase in fracture
as the skull), osteoblast directly elaborate bone without risk’’ [1].
a preliminary cartilaginous anlagen. The modeling phase
allows to reach the peak bone mass towards 25 to 30
years. Modeling can persist in the adult in some cir- The role of bone microarchitecture
cumstances: fracture healing, benign or malignant bone
metaplasia and during the primary phase of adaptation of History
bone to biomaterials. However, areas of minimodeling can
be observed occasionally in adults and are due to a direct Trabecular bone microarchitecture is now recognized as an
bone apposition without preliminary intervention of osteo- important component of bone quality. Other factors are the
clasts. remodeling level, the size of hydroxyapatite crystals, the
Remodeling allows the adaptation of bone to local quality of collagen [15]. The biomechanical value of bone
variations of strains, to hormonal and metabolic changes as a biomaterial depends on both its volume and also on its
during all the rest of the life. In this case, remodeling adapted distribution in the 3D space, that is, its microarchi-
is accomplished by the coordinated action of osteoclasts tecture.
and osteoblasts acting in concert in the form of basic The Scottish naturalist, John Hunter (1728—1793), dis-
multicellular remodeling units (BMU). Bone remodeling is covered by examining animal mandibles, there coexist, at
characterized by a phase of resorption of a piece of bone the same time, areas of bone destruction and areas of bone
tissue that had become mechanically (or metabolically) apposition and also that bone destruction preceded bone
less competent. This phase precedes the formation of a apposition.
new bone structure unit (BSU), which is better adapted In 1867, the German anatomist Hermann von Meyer
to the new conditions. Osteoblasts elaborate BSU dif- received a grant of the Prussian government to study skeletal
ferently in cortical bone (where they are in the form posture. During his research, he studied the orientation of
of cylindrical osteones) and in trabecular bone (where bone trabeculae in the upper femoral extremity and found
these bone packets form curved structures, alike incom- it similar in all subjects. At the time von Meyer presented
plete osteones). BSU themselves are arranged and packed his scientific results, a Swiss engineer (Karl Culmann) real-
in a different way in cortical bone and in trabecu- ized that the drawings representing the spatial distribution
lar bone (where they form trabeculae). This level of of bone trabeculae in the femoral epiphysis had an aston-
organization is known as the bone microarchitecture. A ishing resemblance to the strain lines, which he had used
higher degree of organization is represented by macroar- for designing a crane. Culmann and von Meyer postulated
chitecture of bones themselves: they possess angulations, together a theory saying that the direction of bone trabec-
curvatures, which enable them to adapt to strains and grav- ulae coincides with the strain lines.
ity. Julius Wolf, a German anatomist, confirmed that not
The human skeleton is composed of approximately 20% of only bone trabeculae were aligned with the directions
trabecular bone and 80% of cortical bone. Trabecular bone of the strains, but that their orientations are modi-
has a remodeling level higher than that of cortical bone. Its fied if the strains are changed. For the first time, Wolf
3D microarchitecture is directly conditioned by the mechan- realized that bone microarchitecture represented an adap-
ical strains, which are exerted on it. During childhood, tative answer to mechanical variations. Such adaptability
trabecular bone is primarily made of a dense network of of bone microarchitecture allows a considerable reduc-
plates with, often, an isotropic 3D repartition (i.e., unifor- tion of the bony-material mass necessary to support the
164 D. Chappard et al.

weight of the individual. The theory of adaptation of bone

microarchitecture to strains is now known as the Wolf’s
law.
The German surgeon Wilhem Roux suggested for the first
time that cells contained inside bone could perceive and
provide an answer to the mechanical stresses by controlling
bone resorption and apposition. The American anatomist
John C. Koch showed, in 1917, that bone microarchitec-
ture was optimized: he showed that bone density was
higher in the areas where strains are maximum and he sug-
gested that bone mass is distributed in the best way to
obtain a maximum biomechanical adaptation for a mini-
mal material mass. Then, these concepts were frequently
under-recognized, although some reports by scanning
electron microscopy were published from time to time
[40,41].
The orthopedic surgeon Harold M. Frost, of the Henry
Ford’s Hospital in Detroit, showed that adaptation of bone
microarchitecture is due to bone remodeling. He proposed
the first cellular theories implied in bone remodeling and
showed the differences between bone modeling and remod-
eling. He determined that osteoclastic and osteoblastic
activities were coupled in time and space and proposed
the BMU theory [18]. He showed how strain intensity con-
trolled the nativity and life of BMU (structural adaptations
to mechanical use: SATMU) according to the ‘‘mechanostat’’
theory [16,17].
However, the interdependence of strains and bone
remained under-recognized during decades; a rediscovery
of the importance of bone microarchitecture occurred in
the 1980s, in particular on the impulse of Michael A. Parfitt.
He was the first to propose a mathematical model for
bone microarchitecture by recognizing the importance of
anisotropy, that is, the oriented distribution in space. In
dense cortical bone, osteones are packed such that axes
of all Haversian canals are parallel to the main strain
exerted on the bone shaft (Fig. 1A and B). In trabecular
bone, the bony material realize a network composed of
plates parallel to the strain lines and connected by trans-
verse rods or pillars that ensure the cohesion of the whole
system. The trabecular microarchitecture is evidenced on
X-ray films: plates are vertical in bone submitted to uni-
axial strains (i.e., in the vertebrae, in the tibial plateau)
and create arches when there are strains in various direc-
tions (i.e., femoral head, calcaneus) (Fig. 1C). Parfitt et al.
Figure 1 Microarchitecture of cortical bone, aspect in scan-
also proposed a set of stereological techniques to measure
ning electron microscopy. A. The cortice is porous and made of
trabecular microarchitecture on bone biopsies [33]. How-
osteones compacted together, the Haversian canals are disposed
ever, these techniques are based on the assumption that
parallel to the long axis of the bone, according to the maximum
all trabeculae in the different bones are either in the form
strains direction. The lamellae have been made visible by acid
of plates or rods (‘‘the plate and rod’’ model). One should
etching (the bars stands for 100 ␮m). B. The Haversian canals
note that the distribution of trabeculae finside the vari-
are evidenced by microCT in a semitransparent reconstruc-
ous bones of the skeleton was recognized to be different
tion of a piece of femoral-neck cortex. C. Microarchitecture
[35].
of trabecular bone, in a high-definition radiograph of a
human calcaneus showing the arrangement in arches of the
trabeculae.
Microarchitecture de l’os cortical, aspect en microscopie 100 m). B. Les canaux de Havers sont visualisés en microCT
électronique à balayage. A. L’os cortical est poreux et dans un fragment d’os cortical provenant d’un col fémoral. La
composé d’osteons compactés ; les canaux de Havers sont matrice osseuse a été rendu semi-transparente de façon à bien
disposés parallèlement au grand axe de l’os long (fémur), mettre en évidence les canaux de Havers. C. Microarchitecture
selon la direction des contraintes maximales. Les lamelles ont de l’os trabéculaire dans une radiographie d’un calcaneus
mises en évidence par une gravure à l’acide (la barre représente humain montrant l’arrangement en voûte des travées.
Trabecular bone microarchitecture: A review 165

Parameters currently used to measure trabecular

bone microarchitecture

The most classical histomorphometric parameters currently

used for the description of trabecular bone microarchitec-
ture are all based on Parfitt’s principles of the ‘‘plate and
rod’’ model. These microarchitecture descriptors are: tra-
becular thickness (Tb.Th, in microns), trabecular number
(or more exactly trabecular density) (Tb.N in per millime-
tre) and the trabecular separation (Tb.Sp, in microns). These
parameters are derived from a combination of measure-
ments from trabecular surfaces and perimeters and can be
measured with microscopes equipped with oculars contain-
ing specific reticules or with image analyzers [32].
With the development of microcomputers and the grow-
ing interest for stereology (a branch of mathematics
concerned with the relationships of 2D → 3D), several robust
methods have been proposed to study trabecular microar-
chitecture by using methods independent of surface and
perimeter measurements (i.e., independent of the ‘‘plate
and rod model’’) on digitized images of bone (Fig. 2A).

The trabecular bone pattern factor (Tb.Pf )

This method was proposed by Hahn et al. and is based on
the use of mathematical morphology [21]. The principle of
the method rests on the fact that, in a perfectly connected
structure, concave surfaces are abundant, whereas convex
surfaces are very few. Conversely, in a disconnected struc-
ture, concave surfaces become less abundant and convex
surfaces are then more numerous. Practically, this method
is done by image analysis, performing a dilation of the
original image of the trabecular network and measuring
perimeters and surface areas before and after dilation.
Thus, when a trabecular network is highly disconnected,
the convex surfaces are increased and the dilatation pro-
cess increases the perimeter drastically, while the area is
only moderately affected. This provides low values of Tb.Pf
in a well-connected network and high values when marked
disconnection of trabeculae is present.

Interconnectivity index (ICI)

The method was originally proposed by Le et al. to describe
the connectivity of porous biomaterials, such as corals
Figure 2 Measurement of trabecular bone microarchitec-
[24]. Corals were proposed as substitute biomaterials for
ture by histomorphometric methods based on mathematical
bone grafting since some of them have an exocellular
morphology. A. Digitized image of a bone biopsy showing the
calcium—carbonate matrix that mimics trabecular bone
cortices and the trabecular network. B. The strut analysis sim-
[20]. When applied to trabecular bone, connectivity of the
plifies the trabeculae to the watershed, trabeculae are reduced
marrow cavities can be appreciated on digitized images by
to a line and connection nodes are figures by a dot. C. Star vol-
taking the skeletons of their profiles (i.e., the watershed
ume obtained by sending a seed in the marrow cavities and the
line). Since the skeletonization process is very sensitive to
rays of the star stop when touching a bone surface.
local variations of the boundaries, which produce undesir-
Mesure de la microarchitecture de l’os trabéculaire par des
able dendrites, the skeleton must be pruned to remove the
méthodes histomorphométriques basées sur la morphologie
aberrant terminal ends. On the pruned skeleton, the total
mathématique. A. Image digitalisée d’une biopsie osseuse mon-
number of nodes, node-to-node branches, node-to-free end
trant les corticales et le réseau trabéculaire. B. Analyse des
branches are determined. Also, the number of ‘‘trees’’ is
travées après réduction des travées en une « ligne de partage
obtained, a tree being the structure composed of intercon-
des eaux », les nœuds de raccordement sont figurés par un
nected node(s) with node-to-node and/or node-to-free end
point. C. Méthode du star volume obtenue en plaçant un point
branch(es). The ICI of the bone-marrow cavities combines
de façon aléatoire dans les cavités médullaire et en traçant des
these parameters as previously shown [8]. So, an increased
rayons qui s’arrêtent lorsqu’ils touchent une surface trabécu-
connectivity of marrow cavities (given by a high number of
laire ou endostéale.
nodes and segmental branches associated with a low number
166 D. Chappard et al.

of trees) increases the ICI and corresponds to a fragmenta- The fractal dimension of the trabecular network
tion of the trabecular-bone network. Biological objects have an irregularity and a complexity,
which are often difficult to quantify by the Euclidean geom-
Characterization of the trabecular network (strut etry. The fractal analysis makes it possible to approach
analysis) the complexity of structures and curves. On a 2D sec-
This technique is based on work of Compston and Demp- tion, perimeter of the trabeculae can occupy more or less
ster [11,13]. A method of image skeletonization is applied the section surface according to the complexity of branch-
to the trabeculae with the same algorithms as described ing, connection and more or less regular disposition in
for ICI determination. This allows an identification of the space. . .
various types of trabeculae and a measurement of their con- The fractal dimension D can be measured by the ‘‘boxes
nectivity. Anastomoses or ‘‘nodes’’ between trabeculae are counting’’ method, which consists in superimposing on an
identified; the trabeculae ending with a free terminus are image of the trabecular boundaries, a series of grids made
measured, as well as those connecting two nodes or tra- of similar squares of side ␧ (and mimicking a chessboard)
beculae connected with the cortices (Fig. 2B). Each type of [14]. The number of squares which intercept the trabecu-
strut is allocated to a different color, thus, providing a visual lar boundaries is measured N(␧) and one starts again with a
characterization of the whole trabecular network. In order new grid with a larger ␧. D is obtained by determining the
to obtain a single parameter for easy handling, the node to slope of the straight regression line between log N(␧) and
free-end ratio is determined (N/F) [12]. log ␧ (this is called a Richardson’s plot). The slope D of the
regression line corresponds to the Kolmogorov fractal dimen-
sion. One can measure fractal dimension by other methods:
The star volume
a progressive dilation of the trabecular perimeters provides
This method was largely exploited for the measurement of
the Minskowski-Bouligand’D, the mass radius/lacunarity is
porous materials, in particular of cements and rocks [28].
obtained by positioning circles of growing diameter and
It is based on the analysis of the marrow spaces: starting
counting the number of pixels of the boundaries that are
from a randomly placed seed in the marrow cavity, one can
covered [7].
project rays in all the directions of space (Fig. 2C) [38]. The
All these methods showed are not self-exclusive and
rays stop as soon as they meet a trabecular surface, a cor-
none of them is sufficient to provide a unique parameter
tice or edges of the section. This constitutes a kind of star
that fully describes microarchitecture. We found that it is
and the measurement of the length of each ray of star is
always necessary to use several techniques in association to
done. One sees that the more the network will be discon-
characterize a network trabecular because these different
nected, the more the length of the rays will be important.
techniques do not explore the same components of microar-
If a great number of stars is generated, small perforations
chitecture [7,8]. We found, by using a hierarchical cluster
are highlighted inside the network trabecular. However, this
analysis that three groups of clusters can be identified: one
method is very time consuming and the grid technique is
describing the size of the trabeculae, one describing the
preferred (this method is sometimes referred as the maxi-
medullar cavities and the later corresponding to the branch-
mum intercept length [MIL]): a series of grids are computed
ings of trabeculae. It becomes easy to see that, according
with parallel lines running with various angles running from
to pathophysiological mechanisms, which are implied in the
0 to 2␲. Each grid is stored on the hard disk computer and is
genesis of the various types of bone loss, certain parameters
intersected with the image of the marrow cavities. This pro-
can appear more sensitive than others at earlier times [3,8].
vides linear segments (called chords) superimposed on the
In animal models, measurements of bone microarchitecture
marrow spaces. The cubed length of each chord is then com-
were found more early altered than bone volume (appre-
puted with each grid, so that all directions from 0 to 360◦
ciated by histomorphometry, ash weight and densitometry)
are explored very rapidly. The star volume can be deter-
[29].
mined on the marrow spaces (a high star volume indicates
Nonlinear correlations (e.g., hyperbolic or exponential)
a highly fragmented-bone network); it can also be used on
are frequently met when studying the relationships between
the trabeculae to know their average size.
bone mass (BV/TV) and the various architectural parame-
ters. However, certain parameters (D, E, Tb.Th) are linearly
Euler-Poincaré’s number correlated with bone volume. The inflexion point of the
The method consists in counting the number of particles hyperbolic curves corresponds to a mean Bone Volume of
n present in space trabecular and the number of marrow 11%, a threshold previously assigned by histomorphometric
cavities circumscribed by the trabeculae m. The number of studies to represent a value associated with spontaneous
Euler, E = n − m. Plus the network trabecular is connected, fractures [30]. We found that this threshold corresponds
plus E is weak (even negative). E must be adjusted according to a network whose trabeculae have a mean thickness of
to the surface of space trabecular. The more connected is 70 ␮m. Osteoclasts are able to resorb bone at an average
the trabecular network, the less is E; in this way, negative depth of 40 ␮m: so when osteoclasts erode a thinned trabec-
values are obtained in highly connected systems. ula circumferentially, a perforation can occur and a pillar is
sectioned. This mechanism was evidenced in corticosteroid-
The maximum traveling pathway within the network induced osteoporosis [6] and was also reported in male
The trabecular network can be seen as a labyrinth in which osteoporosis [26]. In males, it is estimated that bone resorp-
one can move in all directions. The more perforations are tion leads to a progressive reduction in the trabecular
disconnecting the trabecular network (thus, merging the thickness upon aging, but the trabecular microarchitec-
marrow cavities), the longer is the pathway [37]. ture and connectivity remain roughly preserved. As soon as
Trabecular bone microarchitecture: A review 167

perforations can occur, they have considerable deleterious

consequences on the biomechanical value of the trabecular
network.
With the development of microcomputers, new mea-
suring instruments have recently appeared allowing the
3D analysis of bone. Micro-MRI are now under develop-
ment and X-ray microtomography (microCT), which allow
a fast exploration and 3D measurement of bone, samples
are available. MicroCT have also been developed for in vivo
analysis of small animals [39] and for analysis of periph-
eral bones, such as the radius and tibia in man [36]. The
synchrotron is also an interesting tool, but it is a very
limited technique due to high costs, difficult accessibil-
ity and the necessity to evaluate small samples [34]. The
standard radiographs, which are used as a routine clin-
ical exam, represent a 2D projection of the trabecular
bone on a silver film or an X-ray sensitive sensor. Sev-
eral groups have tried to appreciate microarchitectural
disorders by describing methods based on image analysis.
Although the 3D → 2D relationships are not fully understood
at the present time, it is likely that there is an inter-
dependence between 2D histomorphometric parameters,
3D microCT data and analysis of plain radiographs [4,19].
Texture analysis of the trabecular network can be appre-
ciated on radiographic images and appears an interesting
and cheap method of appreciation of bone microarchi-
tecture [27]. Techniques of images analysis proposed are
based on the study of run lengths, co-occurrence matrix,
heterogeneity of the pixels’ grey levels and algorithms
based on fractal geometry (skyscrapers method, blankets,
Hurst. . .).
MicroCT allows the measurement of trabecular volume
and trabecular characteristics directly in 3D. In addition,
new parameters have been developed:

• structure model index (SMI) is close to 0 if the trabecular

network is mainly composed of plates, near 3 if rods are
dominating;
• the degree of anisotropy evaluates the orientation of tra-
beculae in space;
• the distribution frequency of the trabecular thicknesses
and marrow cavities width is also of the utmost interest;
• new indices of connectivity have also been proposed (con-
nectivity density, MIL).

However, microCT is only at its beginnings and there

is yet no standardization of parameters between manu-
facturers; furthermore, the validity of some algorithms is

Aspect en microCT de l’os iliaque. A. Chez un jeune sujet : les

Figure 3 MicroCT imaging of iliac bone. A. In a young sub- corticales sont épaisses et le réseau trabéculaire est dense.
ject: the cortices are thick, the trabecular network is dense. B. Dans une ostéoporose postménopausique, notez les per-
B. In a postmenopausal osteoporosis, note the holes inside the forations à l’intérieur du réseau correspondant aux zones
network corresponding to areas of loss of connectivity. C. In de perte de connectivité. C. Dans une ostéoporose masculine
a male with idiopathic osteoporosis, note the conversion of idiopathique, notez la conversion des plaques en piliers et le
plates into rods, although the connectivity is rather well even maintient d’une bonne connectivité, même si les travées sont
if trabeculae are thin. D. In a male with osteoporosis due amincies. D. Dans une ostéoporose masculine idiopathique, due
to multiple risk factors (alcoholism and glucocorticoid treat- à plusieurs facteurs de risque (alcoolisme et traitement par
ment). Note the thinning of the cortices, the considerable glucocorticoïdes). Notez l’amincissement considérable des cor-
disorganization of the trabecular network with area without ticales, la désorganisation maximale du réseau trabéculaire et
trabeculae. la disparition complète des travées dans certaines zones.
168 D. Chappard et al.

questionable. In particular, it appears that algorithms used Evolution with the age of bone trabecular microarchitec-
for thickness measurements are strongly influenced by the ture seems also different in normal man as evidenced using
shape of the measured objects themselves: nodes (zones histomorphometric methods. Perforations of bone trabecu-
of connectivity between trabeculae) have a considerable lae are less frequent in man so that connectivity is better
influence on thickness values and can lead to erroneous preserved in the males [31].
conclusions [5,9]. MicroCT has also the disadvantage of The study of the bone microarchitecture by histomor-
providing no information on cellular activities, but offers phometry has brought important data to knowledge of the
the advantage of being nondestructive for bone samples, pathophysiology of the disease. During primitive or sec-
which can thus be processed by conventional histological ondary osteoporosis, there is a marked reduction of the
methods. trabecular-bone volume, in the thickness and number of
trabeculae, but also a marked disorganization of the tra-
becular microarchitecture: a reduction in the number of
Alterations of trabecular microarchitecture
nodes (on the strut analysis), an increase in the number of
free ends (bone trabeculae with end termini), an increase of
During ageing ICI and star volume of the bone-marrow spaces. An impor-
tant and sudden rise in these architectural indices occurs
In the young, the trabecular network is dense and plexi- when the trabecular bone volume becomes lower than 11%
form. During ageing, bone trabeculae are thinned because or the thickness of the trabeculae lower than 70 ␮m [6]. A
of a constant osteoblastic depression. Like any connective logistic regression study, done in 108 osteoporotic males,
cell, osteoblasts encounter a reduced capacity for matrix confirmed that the relative risk of vertebral fractures was
synthesis (collagen and non-collagenic proteins regularly strongly influenced by the quality of bone microarchitec-
decrease), leading to a progressive conversion of the plates ture [26]. After adjustment for age, body mass index and
into rods (Fig. 3A and B). femoral density, the occurrence of fractures remained asso-
ciated with microarchitectural indices, with relative risks
In female varying between 1.7 and 3.2 for one S.D. variation of the
connectivity parameters.
According to etiologic factors, it seems that microar-
At the menopause, the estrogenic deficiency leads to an
chitectural abnormalities of the trabecular network are
increase in several cytokines (IL-6, IL-7, TNF␣. . .), leading
different [2]. In glucocorticoid-induced osteoporosis, tra-
to a stimulation of the osteoclastic activity [10]. The num-
beculae become thinner, but the overall connectivity is
ber of activated BMU increases and osteoclasts can erode
preserved. However, specific aspects of plate thinning can
trabeculae since their lifespan is increased (inhibition of
be observed in microCT with multiple minute perforations
apoptosis) [22]. The consequence in an increased in the
occurring in their center [5]. In hypogonadic patients, the
number of trabecular perforations (Fig. 3C), which disor-
trabeculae remain thick, but disorganized by holes in the
ganize the 3D microarchitecture [23]. Some authors have
network. In male osteoporosis, the deleterious effect of risk
proposed the term ‘‘killer osteoclasts’’ to indicate this phe-
factors is additive on bone microarchitecture. For example,
nomenon responsible for an acceleration of bone remodeling
a subject presenting a hypogonadism and alcoholism will
with a bone loss, which can reach − 2% per year during the
have a microarchitecture much more altered than a subject
menopausal period leading to a − 20 to − 30% reduction of
presenting only one of these risk factors. The number of
the initial bone mass.
fractures parallels the number of fracture risks as well [25].

In male
Conclusion
In male, etiologic factors which condition bone loss are
multiple, intricate and the diagnosis is often much more Trabecular microarchitecture is a very important aspect
complex than in female. The peak bone mass is acquired just of bone fragility. It is now recognized as one of the
at the beginning of the third decade and is approximately bone-quality factors that can explain the occurrence of
30% higher than that of females because of the largest fractures. A survey of the scientific literature in the Med-
diameter of the bones. Prepubertal growth, which largely line database indicates that the number of papers including
conditions the size of bones, is on average two years longer ‘‘bone microarchitecture’’ or ‘‘bone structure’’ is grow-
in man. The long bones diameter and vertebral surfaces ing exponentially. Seven papers included one of these key
are thus approximately 20 to 25% higher, contributing to words in 1970, thirty in 1987 (when the first papers deal-
an increased biomechanical resistance. Tomodensitometric ing with microarchitecture were published) to 515 in 2007.
studies have shown that trabecular-bone loss during ageing Aside to microarchitecture, other factors are now recog-
is similar in both genders, particularly in the spine (if one nized and assembled under the umbrella term of bone
excepts the menopausal period). Evolution of long bones is, quality [15]. Bone quality includes the remodeling rate,
on the other hand, different: cortical porosity and endosteal the mineralization degree and its heterogeneity, the size of
resorption, which occur in both genders, are reduced in man hydroxyapatite crystals, the collagen and non-collagenous
while periosteal apposition is more important. So the cross proteins composition, the osteocyte viability and the micro-
section of long bones, a factor of biomechanical resistance, or nanomechanical resistance. It is likely that abnormalities
increases with the age in man, particularly at the femoral in any of these factors can provoke bone fragility by acting
neck. either at tissular, cellular or molecular level.
Trabecular bone microarchitecture: A review 169

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