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European Journal of Histochemistry 2010; volume 54:e48
[page 226] [European Journal of Histochemistry 2010; 54:e48]
Subcutaneous adipose tissue
classification
A. Sbarbati,1D. Accorsi,2D. Benati,1
L. Marchetti,2G. Orsini,3G. Rigotti,4
P. Panettiere2
1Department of Neurological,
Neuropsychological, Morphological and
Motor Sciences, Human Anatomy and
Histology Section, University of Verona
2Department of Specialised and
Anaesthesial Surgery Sciences, University
of Bologna
3Department of Clinical Sciences and
Stomatology, Marche Polytechnic
University, Ancona
4Second Division of Plastic and
Reconstructive Surgery, the Institute for
Burns, and Regional Center for Breast
Reconstruction, Ospedale Maggiore,
Verona, Italy
Abstract
The developments in the technologies based
on the use of autologous adipose tissue attract-
ed attention to minor depots as possible sam-
pling areas. Some of those depots have never
been studied in detail. The present study was
performed on subcutaneous adipose depots
sampled in different areas with the aim of
explaining their morphology, particularly as far
as regards stem niches. The results demon-
strated that three different types of white adi-
pose tissue (WAT) can be differentiated on the
basis of structural and ultrastructural features:
deposit WAT (dWAT), structural WAT (sWAT)
and fibrous WAT (fWAT). dWAT can be found
essentially in large fatty depots in the abdomi-
nal area (periumbilical). In the dWAT, cells are
tightly packed and linked by a weak net of iso-
lated collagen fibers. Collagenic components
are very poor, cells are large and few blood ves-
sels are present. The deep portion appears
more fibrous then the superficial one. The
microcirculation is formed by thin walled cap-
illaries with rare stem niches. Reinforcement
pericyte elements are rarely evident. The sWAT
is more stromal; it is located in some areas in
the limbs and in the hips. The stroma is fairly
well represented, with a good vascularity and
adequate staminality. Cells are wrapped by a
basket of collagen fibers. The fatty depots of
the knees and of the trochanteric areas have
quite loose meshes. The fWAT has a notewor-
thy fibrous component and can be found in
areas where a severe mechanic stress occurs.
Adipocytes have an individual thick fibrous
shell. In conclusion, the present study demon-
strates evident differences among subcuta-
neous WAT deposits, thus suggesting that in
regenerative procedures based on autologous
adipose tissues the sampling area should not
be randomly chosen, but it should be oriented
by evidence based evaluations. The structural
peculiarities of the sWAT, and particularly of its
microcirculation, suggest that it could repre-
sent a privileged source for regenerative pro-
cedures based on autologous adipose tissues.
Introduction
In obese individuals, subcutaneous fat can
represent the most voluminous structure of
the body and several data suggest that it plays
a role in the pathogenesis of some severe dis-
eases.1,2 Moreover, in regenerative medicine,
methods based on autologous subcutaneous
adipose tissues are getting more and more
popular.3In fact, among the various stem pop-
ulation identified by now, the mesenchymal
adipocyte line proved to be the most promising
in the perspective of clinical appliances, due to
its abundance and availability. Subcutaneous
adipose tissue represents an almost unlimited
reservoir of stem cells that can be harvested
with minimally invasive procedures.4It is note-
worthy that unlike all other body tissues, fat
can significantly increase its mass with age.
Moreover, an increasing number of experi-
mental studies highlighted the huge neo-
angiogenic and immunomodulatory potentials
of adipose stem cells, promoting their use in
the therapy of ischemic and autoimmune dis-
eases.5Some animal model based studies and
preliminary clinical trials demonstrated the
therapeutic efficacy in neurologic and cardio-
vascular pathologies. Moreover, some clinical
trials proved the lack of any of the complica-
tions pointed out by different stem cells regen-
erative therapy approaches.6The currently
more advanced clinical application is in plastic
surgery where adipose cells revealed to be able
to correct several pathologies and in particular
scar lesions.7
In such a context, the complex made of cell,
extracellular and biochemical elements whom
the adipose cell interacts with in its natural
micro-environment (niche), proved to play a
critical role. The implant of autologous stem
cells enriched lipoaspirate rather than isolated
stem cells could configure as the substitution
of an atrophic niche with a physiologic one,
where the stem niches can be forced to per-
form their normalizing role on the receiving
tissue. The development of stem niches based
therapies emphasizes the need for a precise
characterization of the stromal components of
subcutaneous adipose tissues, which is the
most common source of stem niches.
Despite the metabolic and molecular behav-
ior of these elements have already been char-
acterized,8a comparative analysis of the stro-
mal components of adipose tissues (in partic-
ular of the collagenic scaffold wrapping the
adipocytes in the different sites) has never
been performed.
The lack of scientific evidence represents a
serious knowledge gap so that the choice of a
sampling site is based only on mere empirical
or even random considerations.
Still, morphologic studies carried out until
now generally gave great relevance to the
abdominal fatty depots and only paid a scarce
attention to the minor ones.
Information about such a structural organi-
zation cannot be obtained by means of bio-
chemical techniques or optical microscopy, but
requires ultrastructural evaluations. The fea-
tures of such a scaffold could be the reason for
the different resistance of adipocytes to the
mechanical stimulations during harvesting,
isolation and implantation.9
Moreover, the knowledge about the micro-
circulation and the stem cells niches associat-
ed to the different fatty depots is totally incom-
plete. Ultrastructural analysis techniques
never used in the past are seemingly mandato-
ry for the study of these parameters too.
In the present study we therefore analyzed a
high number of subcutaneous adipose tissue
samples harvested from the most common
sources of adipose stem cells to determine
their features and to highlight the tissue
parameters that address them to a preferential
use in the various conditions in reconstructive
medicine. In particular, an integrated protocol
of transmission and scan electron microscopy
was used, providing an accurate tridimension-
al and sub-microscopic evaluation of these
Correspondence: Prof. Andrea Sbarbati,
Dipartimento di Scienze Neurologiche, Neuro -
psicologiche, Morfologiche e Motorie, Sezione di
Anatomia e Istologia, Università di Verona, stra-
da Le Grazie 8, 37134, Verona, Italy.
Tel. +39.045.8027155 - Fax: +39.045.8027163
E-mail: andrea.sbarbati@univr.it
Key words: adipocyte, adipose stem cells, fat
transplantation, liposuction.
Received for publication: 19 August 2010.
Accepted for publication: 6 October 2010.
This work is licensed under a Creative Commons
Attribution 3.0 License (by-nc 3.0).
©Copyright A. Sbarbati et al., 2010
Licensee PAGEPress, Italy
European Journal of Histochemistry 2010; 54:e48
doi:10.4081/ejh.2010.e48
[European Journal of Histochemistry 2010; 54:e48] [page 227]
structures. The study of subcutaneous white
adipose tissue by means of optical microscopy
doesn’t allow an adequate visualization of the
structural tissue organization. In fact, the
large dimensions of the cells, whose cytoplasm
is occupied almost totally by a unique triglyc-
eride drop, generates an apparently amor-
phous pattern inside which it is virtually
impossible to understand the features of the
organization. The intracellular space appears
compressed among the triglyceride masses
and its aspect appears not differentiable
among the different tissue areas. Optical
microscopy alone revealed scarcely useful also
in the characterization of both the connectival
stroma and the vasculo-stromal component of
subcutaneous adipose tissue. A protocol based
on comparative evaluations of scanning elec-
tron microscopy (SEM) and transmission elec-
tron microscopy (TEM) seemed to be more
suitable for such aims. These techniques, in
fact, can provide complementary information
about the tridimensionality of collagenic and
stem-vascular structures and about their fine
composition.
Materials and Methods
Forty female patients with age ranging from
30 to 67 years (average: 51.3 ys) underwent fat
harvesting from September to October 2009 for
autologous fat implant. A mixture of 0.5% xylo-
caine + epinephrine 1:200,000 in saline solu-
tion was injected before suction. Fat harvest-
ing was performed by a 3 mm cannula (1-hole,
bullet tip) connected to a 10 cc syringe for vac-
uum; fat was then gently washed in saline and
decanted. Centrifugation was not performed.
Harvesting was performed in 10 different sites:
arms, armpits, pectoral, periprosthetic tissue
(breast prostheses, irradiated or non-irradiat-
ed), abdomen, pubic, hips, trochanters, inner
face of the knees and heels.
For ultrastructural examination, we used
methods applied in previous studies on white
adipose tissue (WAT): specimens withdrawn
in these works were also used as controls.1
For TEM, parts of the specimens were
immediately fixed in 2.5% glutaraldehyde in
Sorensen buffer for 2 h, postfixed in 1% osmi-
um tetroxide in Sorensen buffer for 1 h dehy-
drated in graded acetones, embedded in Epon-
Araldite and cut with an Ultracut E Ultra -
microtome (Reichert, Wien, Austria).
Ultrathin sections were stained with lead cit-
rate and observed in an EM10 electron micro-
scope (Zeiss, Oberkocken, Germany). The
semithin sections were stained with Toluidine
blue.
For SEM the specimens were fixed in 2.5%
glutaraldehyde in Sorensen buffer for 2 h, post-
fixed in 1% osmium tetroxide in Sorensen
buffer for 1 h and dehydrated in graded ace-
tones (Fluka, St. Louis, MO, USA). The speci-
mens were then treated by critical point dryer
(CPD 030; Balzers, Liechtenstein) and coated
by gold, mounted on stubs and observed in an
XL 30 ESEM (FEI- Philips). Data about
adipocyte size were obtained by SEM examina-
tion.
Results
The combined analysis by transmission and
scan electron microscopy allowed us to define
the three main different patterns in the subcu-
taneous WAT described below.
Fatty depots appear to be differentiable into
distinct adipose tissue typologies. However, it
should be clarified that also in the same depot
there can be evident differences that can be
correlated to the superficial or deep localiza-
tion or to the patient’s age. In general, the
depots subject to mechanic stresses present a
larger connective component. There are not
only qualitative differences, but also quantita-
tive ones and intermediate states among the
different typologies can be evidenced.
It should also be clarified that, inside larger
depots, the aspect could be inhomogeneous. In
the abdomen and in the hips, for example, the
deep layer appeared richer in fibrous struc-
tures. Moreover, in older patients there is a
larger amount of collagen than in younger
ones. Such an increase appears to be both an
increase in the more coarse connectival mesh
and a thickening of the peri-adipocyte meshes.
The average diameter tends to increase with
age, while the number of peri-vascular stem
cells tends to reduce. In the older patients a
moderate thickening of vascular walls was also
observed, with duplicated basal membranes
and homogeneous thickenings at times.
Classification of subcutaneous
depots
Subcutaneous depots only apparently pres-
ent structural and ultrastructural homogeneity.
Actually, they form a very polymorphous and
variegate sub-family of tissues due to the dif-
ferent roles played by each single district.
In general, three kinds of adipose tissues
can be distinguished, based on their structural
and ultrastructural features. Such types differ
by both the adipocyte and the vasculo-stromal
components. Ranging from type one to three, a
progressive increase in stroma (with different
features) can be observed. However, it should
be underlined that in different areas, the indi-
vidual depots can be made by mixtures of dif-
ferent types of adipose tissues.
Type #1 deposit white adipose tissue
The type #1 adipose tissue (Figure1 A,E) is
located essentially in large depots in the
abdominal area (peri-umbilical). It is a typical
non-lobulated adipose tissue that could be
defined as metabolic fat due to its large lipidic
mass and its very poor collagenic component
(non-stromal). It is characterized by large adi-
pose cells: the average diameter, in our exper-
imental conditions, was 95 μm. It presents few
capillaries in comparison to other WATs. The
TEM demonstrates that cells are closely packed
while at SEM a weak reticulum of isolated col-
lagen fibers is visible. In particular, at SEM the
fibrillar network connecting the contiguous
adipocytes is extremely weak or virtually
absent. These cells appear not to be wrapped
by a real collagen fibers basket, which can
instead be found in other types of WAT. The
adipose cells form a sort of a syncytium where
the extracellular space is extremely thin. The
microcirculation is formed by thin walled cap-
illaries with rare stem niches. Pericyte rein-
forcement elements are rarely evident. These
adipocytes, not being separated by collagen,
tend to adhere each other with parallel mem-
brane plates. In the older patients the mesh
was thicker, taking a coarse aspect with large
shoots forming a loose meshed reticulum.
Peri-vascular macrophages are not infrequent.
Type #2 structural white adipose
tissue
The type #2 adipose tissue (Figure 2 A,D) is
more polymorphous and variable from site to
site, as it plays different roles based on the
relationships with the surrounding structures.
Such variability can also be appreciated as dif-
ferences in tissue consistency during harvest-
ing. In general, it is a more stromal fat and it is
located in much limited adipose areas, usually
rich of muscular tissue.
The type #2 fat is characteristic of more
localized depots, where its function goes
undoubtedly beyond the depot itself: in such
areas, the adipose tissue appears mainly final-
ized to mould, that is to give a shape to the
structure. The fat in trochanters, sovrapubic
area, arm pits, inner faces of the knees, thighs,
arms, pectoral and mammary areas and hips all
pertain to this group. The average diameter of
adipocytes is smaller than in dWAT: about 81
μm. Greater diameters can be found in the
inner faces of the knees (92 μm) and in the
trochanters (86 μm).
It is a non-lobular adipose tissue with a vari-
able collagenic component, often forming
coarse shoots. They appear relatively easy to
dissociate due to their structure. At times the
stroma appears fairly good and well vascular-
ized. Staminality is generally fair. In fact, some
elements related to the basal membrane (poor-
Original paper
[page 228] [European Journal of Histochemistry 2010; 54:e48]
ly differentiated or in course of differentia-
tion) can be found in the peri-capillary spaces.
Such elements are generally rich of polyribo-
somes and have few other organules made of
isolated endoplasmic reticulum cisternae.
Moreover, capillaries can show basal mem-
brane duplications or thickenings, mostly in
aged people. Rare macrophagic elements are
generally present. Among the various depots,
some peculiar aspects can be noticed in those
undergoing specific mechanic stimulations in
the lower limbs. For example, the depots on the
inner faces of the knees and in the tro -
chanteric areas present a quite thin connecti-
val mesh, almost mesenchymal-like. In scan
images, the peri-adipocyte baskets are charac-
terized by large meshes made of isolated colla-
gen fibers. Such basket often tends to detach
from the plasmalemma of the adipocytes (that
in these areas appears uniformly smooth).
Type #3 fibrous white adipose tissue
The type #3 adipose tissue (Figure 3 A,C)
has a remarkable fibrous component and is
characterized by a well defined mechanic func-
tion. It can generally be found in areas where
the mechanic stress can be considerable.
Adipocytes are therefore smaller, with a thick
fibrous shell wrapping them one by one. At
SEM, a tight reticulum of thickened collagen
fibers is visible in a thick layer around the
adipocytes. Such a reticulum can be visible
also at optical microscopy, but it appears clear-
ly only at TEM. This kind of adipose tissue,
characterized by a conspicuous prevalence of
collagenic stroma can present in lobular or
non-lobular subtypes.
Lobular subtype
It can be found for example in the calcaneal
fat pad; it is a lobular adipose tissue with micro
and macro chambers delimited by connective
septa. The tissue is well vascularized, with capil-
laries characterized by a thick endothelium,
duplicated basal membranes and covered by
velamentous cells. The adipocytes are large (97
μm) and covered by thick connective sheaths
made of very thick collagen bundles. At SEM, the
sheaths appear as compact, high density layers
that prevent the single meshes to be caught a
glimpse of due to the tight apposition of collagen
fibers. However, the outer surface of the basket
appears almost regular and easy to dissociate
from the stromal collagen. Therefore, the
sheaths appear as structures with an evident
morphologic identity, closely associated to the
plasmalemma of the adipocyte from which they
seem to be separated by no visible space at TEM.
Non-lobular subtype
It is a tissue with a maximum degree of
fibrosis. It can be found, for example, in the
periprosthetic capsules (both irradiated and
non irradiated). It is a hard adipose non-lobu-
lated tissue, with a strong stromal component.
Vascularization is florid and macrophages and
at times elongated elements with a poor lipidic
content (that can be referred to adipocyte line
in course of differentiation), can be found
around microvessels.
Discussion
In the present work, the comparative sys-
tematic analysis of human subcutaneous tis-
sues performed with ultrastructural methods
also in areas never studied before led to the
description of a structure never described
before: the collagenic peri-adipocyte basket.
Such a structure probably plays an important
role in the preservation of cell integrity and it
can consequently influence the results in fat
harvesting procedures and in autologous fat
transplant. Based on the morphology of the
basket, three different types of subcutaneous
WATs can be patently identified and it is not
surprising that the areas more subject to
mechanic stress present more developed colla-
genic peri-adipocyte baskets.
An important data emerging from the pres-
ent study is therefore the polymorphism of the
subcutaneous adipose tissue. In fact, despite
the common idea that fat is contained in an
almost homogeneous cavity, the comparative
systematic analysis of human samples demon-
strated that the adipose organ appears as a
very differentiated entity. This leads to realize
that it should be more appropriated to use the
terms subcutaneous adipose tissues instead of
subcutaneous adipose tissue. The data
obtained by groups of patients of different ages
suggest that such a specialization could be in
part related to the length of human life as it is
less evident in the common laboratory species,
whose average life span is generally no longer
than 24 months. It appeared to be very difficult
to appreciate these differences at mere optical
microscopy and this is probably the main rea-
son why they have never been underlined in
preceding studies led with different aims. The
differences found seem to be mainly related to
Original paper
Figure 1. Abdominal adipose tissue: the tissue is characterized by large adipose cells and a poor
collagenic component. (A) Light microscopy (scale bar: 15 µm). (B)SEM (scale bar: 50 µm).
(C) SEM (scale bar: 20 µm). The adipocytes are surrounded by a thin capsule of collagen
fibres. Panel D, TEM (scale bar: 2000 µm). Panel E, TEM (scale bar: 500 µm). TEM images
confirm that only sparse collagen fibres surround the adipocytes.
[European Journal of Histochemistry 2010; 54:e48] [page 229]
the composition of the stromal compartment
and it patently emerged that the differences
can be substantially connected to the function-
al specializations of the depots in the various
sites. These results about regional differences
in morphology confirm the data indicating that
there are regional differences in the metabo-
lism of subcutaneous fatty depots.10,11 Lipids are
mobilized at a slower rate but synthesized at a
higher rate in the femoral than the abdominal
region. Fasting is accompanied by an
increased rate of fat mobilization and a
decreased rate of fat synthesis in all fatty
depots. These changes are, however, more pro-
nounced in abdominal than in femoral fat.
There are also regional differences in the hor-
monal regulation of fat metabolism in obesity.
The action of insulin is most pronounced in
the femoral region whereas the one of cate-
cholamines is most marked in the abdominal
area. The regional differences in hormone
action are further enhanced during therapeu-
tic fasting.10 Abdominal adipocytes from
females showed a 40 times lower alpha 2-
adrenergic antilipolytic sensitivity than did
gluteal adipocytes.11
While previous studies mainly focused on
the adipocyte compartment, the present study
aimed at a detailed analysis of the stromal
compartment. Based on TEM and SEM analy-
sis, we could define three main types of subcu-
taneous fat that can be named as dWAT, sWAT
and fWAT.
The main difference among the three types
is definitely the morphology of a structure that
was never clearly identified before: the peri-
adipocyte collagenic basket. Such a structure
appears seemingly important in determining
the mechanic features of the tissue and pres-
ents patent differences in the three types. In
the dWAT, the basket is incomplete and
extremely weak so the membranes of the
adipocytes are tightly adherent. Usually, only
isolated collagen fibers settle in the virtual
space. As whole, the tissue appears as a sort of
syncytium made of large dimension tightly
adherent elements. So, such an aspect appears
characterized by a huge lipidic collection with
a poor stromal component. The difficulty of dis-
sociation of the adipocyte depots during har-
vesting could be related to the tight adherence
among the cells. This could also imply a higher
cellular damage during harvesting because
traction and suction could break the cells
instead of separating them.
Further studies are necessary to confirm
this hypothesis. The features of the microcir-
culation indicate that the dWAT is a slow
turnover tissue with a low staminality, even if
data from other techniques are mandatory to
confirm morphologic findings.
In the sWAT, the collagenic peri-adipocyte
basket is well structured and associated to an
on average more cellular microvascular com-
partment compared to what was observed in
the large abdominal depots. This could be
related to the mechanic stress that the depots
or part of them are subject to. In fact, sWAT is
typically located in areas that underwent to a
more pronounced exposition to traumatism
with respect to dWAT. It should be pointed out
that the sWAT takes different morphologies
depending on the depots and on the age of the
patient.
In the fWAT, the collagenic peri-adipocyte
basket appears as enormously thick and made
of collagen parallel bands. Such feature is
added to an absolutely peculiar microcircula-
tion morphology, characterized by thick walled
vessels with, at times, duplicated basal mem-
branes. These features are probably related to
the peculiar tissue mechanic performances
that can be found in pathologic or, more rarely,
physiologic situations such as in the calcaneal
pad. In this case, it is evident that the function-
al performances under load of ”soft” elements
Original paper
Figure 2. Structural adipose tissue. The type
2 adipose tissue is characterized by a variable
collagenic component. (A) light microscopy
(scale bar: 15 µm). (B) TEM (scale bar: 5 µm).
The picture shows a stroma rich in collagen
fibers and well vascularized. (C) SEM (scale
bar: 35 µm). In this area the connective cap-
sule is thin and partially detached. (D) SEM
(scale bar: 20 µm). The picture shows
adipocytes covered by a relatively dense con-
nective capsule.
Figure 3. Fibrous adipose tissue with a
remarkable fibrous component. (A) Light
microscopy (scale bar: 15 µm). (B) SEM
(scale bar: 10 µm). A tight reticulum of thick-
ened collagen fibers is visible in a thick layer
around the adipocytes. (C) TEM (scale bar: 5
µm). The adipocytes are covered by thick con-
nective sheaths made of very thick collagen
bundles. a, adipocyte; c, connective tissue; v,
blood vessel; e, endothelium; ↑collagen bun-
dle; *pericellular connective capsule.
[page 230] [European Journal of Histochemistry 2010; 54:e48]
like adipocytes would be unbelievable without
a noteworthy collagenic apparatus. It is signif-
icant the fact that despite the absolutely pecu-
liar features of this tissue, it has never been
ultrastructurally studied in detail. The use of
such methodologies clearly shows that the
main feature of fWAT is not only a greater
amount of collagen, but rather mainly its dif-
ferent set-up that takes the shape of collagenic
peri-adipocyte membranes. The microcircula-
tory morphology is also absolutely peculiar due
to the presence of some ultrastructural aspects
like the endothelial thickness, the presence of
perivascular elements, but mostly the duplica-
tion of basal membranes, suggesting a rapid
cell turnover, probably in response to chronic
traumatism.
In conclusion, the present study describes a
new morphologic structure: the peri-adipocyte
basket. It demonstrates the existence of differ-
ent varieties of WAT and that noteworthy dif-
ferences are present in the connectival and
micro-vascular compartments. Moreover, this
work provides practical indications for opti-
mization of harvesting procedures in the treat-
ments based on autologous WAT.
Our data suggest that the best results in
harvesting procedures and in subsequent
implant can probably be obtained by the sWAT.
In this tissue the elements are separated by a
thin collagen voile and the microcirculation is
rich of stem elements. Such features could be
related to the chronic stimulation status to
which the depots undergo leading to a cyto-
plasmatic degree of activation of the pericyte
elements. This makes sWAT the ideal tissue
for staminality restoring therapies based on
the creation of ectopic stem niches.12
In particular, our data suggest as particular-
ly noteworthy those sWAT depots where the
collagenic mesh is particularly weak, such as
the trochanteric ones or those in the inner
face of the knees. Moreover, data from SEM
seem to demonstrate that in such depots the
collagenic sheaths can easily be detached from
the adipocytes. This feature could be a further
factor explaining the optimal consistency of
the tissue. The weakness of the connectival
baskets and the easy detachability of adipo -
cytes seem to favor tissue harvesting. In our
experience in these depots the dissociability of
the adipose elements is higher.
Finally, these variants of sWAT have a strong
vasculo-stromal fraction, very rich in already
activated stem cells. Such features are proba-
bly determinant factors in the process of recon-
structing ectopic stem niches in the damaged
tissues. Therefore, this work suggests that, in
regenerative procedures based on transplant
of autologous adipose tissues, the site of har-
vesting should not be randomly chosen, but it
should be indicated by evidence based evalua-
tions. The structural peculiarity of sWAT, and
in particular of its microcirculation, suggests
that this tissue could represent a privileged
source for harvesting in regenerative proce-
dures based on autologous adipose tissues.13,14
References
1. Sbarbati A, Osculati F, Silvagni D, Benati
D, Galiè M, Camoglio FS, et al. Obesity and
inflammation: evidence for an elementary
lesion. Pediatrics 2006;117:220-3.
2. Cinti S. The adipose organ. 1999 Ed.
Kurtis, Milan, Italy.
3. Rigotti G, Marchi A, Sbarbati A. Adipose-
derived mesenchymal stem cells: past,
present, and future. Aesthetic Plast Surg
2009;33:271-3.
4. Krampera M, Marconi S, Pasini A, Galiè M,
Rigotti G, Mosna F, et al. Induction of neu-
ral-like differentiation in human mes-
enchymal stem cells derived from bone
marrow, fat, spleen and thymus. Bone
2007;40:382-90.
5. Constantin G, Marconi S, Rossi B, Angiari
S, Calderan L, Anghileri E, et al. Adipose-
derived mesenchymal stem cells amelio-
rate chronic experimental autoimmune
encephalomyelitis. Stem Cells 2009;27:
2624-35.
6. Rigotti G, Marchi A, Stringhini P, Baroni G,
Galiè M, Molino AM, et al. Determining the
Oncological Risk of Autologous
Lipoaspirate Grafting for Post-Mastectomy
Breast Reconstruction. Aesthetic Plast
Surg 2010;34:475-80.
7. Rigotti G, Marchi A, Galiè M, Baroni G,
Benati D, Krampera M, et al A. Clinical
treatment of radiotherapy tissue damage
by lipoaspirate transplant: a healing
process mediated by adipose-derived adult
stem cells. Plast Reconstr Surg
2007;119:1409-22.
8. Peroni D, Scambi I, Pasini A, Lisi V, Bifari
F, Krampera M, et al. Stem molecular sig-
nature of adipose-derived stromal cells.
Exp Cell Res 2008;314:603-15.
9. Galiè M, Pignatti M, Scambi I, Sbarbati A,
Rigotti G. Comparison of different cen-
trifugation protocols for the best yield of
adipose-derived stromal cells from lipo -
aspirates. Plast Reconstr Surg 2008;
122:e233-4.
10. Arner P. Site differences in human subcu-
taneous adipose tissue metabolism in obe-
sity. Aesthetic Plast Surg 1984;8:13-7.
11. Wahrenberg H, Lönnqvist F, Arner P.
Mechanisms underlying regional differ-
ences in lipolysis in human adipose tissue.
J Clin Invest 1989;84:458-67.
12. Sbarbati A, Galiè M. The niche theory for
fat graft survival. Pages 15-30 in: Fat injec-
tion. From filling to regeneration.
Coleman SR and Mazzola RF, eds. 2009,
Quality Medical Publ., Inc, St. Louis, MI,
USA.
13. Panettiere P, Marchetti L, Accorsi D, Del
Gaudio GA. Aesthetic breast reconstruc-
tion. Aesthetic Plast Surg 2002; 26:429-35.
14. Panettiere P, Marchetti L, Accorsi D. The
serial free fat transfer in irradiated pros-
thetic breast reconstructions. Aesthetic
Plast Surg 2009;33:695-700.
Original paper
