Comptes Rendus Chimie

Christophe Poulard

Arnaud Dessombz

Michel Daudon

Dominique Bazin

Duration of JJ stent in situ is critical: An ultrastructural and mechanical investigation

Shweta Agarwal

Sergio Bertazzo

lable at ScienceDirect
C. R. Chimie 19 (2016) 1605e1609Contents lists avaiComptes Rendus Chimie
www.sciencedirect.comAccount/RevueNew paradigms in cardiovascular calcification
Shweta Agarwal a, Sergio Bertazzo b, *
a Department of Materials, South Kensington Campus, Imperial College, London, SW7 2AZ, UK
b Department of Medical Physics & Biomedical Engineering, University College London, Malet Place Engineering Building, London, WC1E
6BT, UKa r t i c l e i n f o
Article history:
Received 27 February 2015
Accepted 29 September 2015
Available online 21 February 2016
Keywords:
Vascular calcification
Biomineralisation
Electron microscopy
Calcium
Phosphate* Corresponding author.
E-mail addresses: s.agarwal12@imperial.ac.uk (S.
ucl.ac.uk (S. Bertazzo).
http://dx.doi.org/10.1016/j.crci.2015.09.013
1631-0748/© 2015 Académie des sciences. Publishea b s t r a c t
Out of several concurrent hypotheses that attempt to explain the development of calcific
lesions in vascular tissues, the most widely accepted is based on the formation of bone-like
tissue. Conversely, a study recently published on a materials science journal shed new light
on the nature of cardiovascular calcification. The results have shown that cardiovascular
calcification found in tissues affected by different calcific diseases is formed from the same
nano/micro calcified spherical particles, which are also the first calcified structure that
could be detected in vascular tissue. Moreover, cardiovascular calcification is not formed
mainly by bone tissue but, surprisingly, by a not previously described, highly crystalline
calcium phosphate material. By combining biology, materials science and chemistry, the
new results have generated fundamental insights into the nature of cardiovascular calci-
fication. This perspective summarizes these findings and epitomizes the scientific
approach it has used to address important clinical questions.
© 2015 Académie des sciences. Published by Elsevier Masson SAS. All rights reserved.1. Introduction
Calcification in the cardiovascular system is a common
mineral metabolic disease that contributes to many of the
approximately 17 million deaths per year caused by car-
diovascular disease [1]. The burden of calcific disease is
relatively larger in male individuals and increases with
advancing age, diabetes mellitus, hypertension, smoking,
elevated low-density lipoprotein levels, metabolic syn-
drome and renal dysfunction [2]. The cardiovascular tissues
more commonly affected include the aorta, femoral arteries
and aortic valves [3e5]. In cardiac valves, calcification is
characterized by calcific lesions on the valve cusp, resulting
in an impaired movement of the leaflets. Pathological
mineralization in arteries can lead to stenosis throughAgarwal), s.bertazzo@
d by Elsevier Masson SAS. Athickening and stiffening of tissues, reducing blood flow
and eventually resulting in heart failure [6,7].
Calcification associated with atherosclerosis may
significantly increase health concerns. Calcification nuclei
have been associated to cell death and atherosclerotic intra
plaque hemorrhages. The differences in mechanical prop-
erties between the mineral and the tissue can actually
provoke hemorrhages. Moreover, the calcification found in
the lipid core of lesions can produce micro fractures, which
in turn can lead to acute thrombosis and even fatal
myocardial infarction [8,9].2. Existing models of cardiovascular calcification
Cardiovascular calcific disease was described as a pas-
sive degenerative process that occurs due to deterioration
of tissues caused by the stress and strain of cardiac func-
tion. More recently, research associated with molecular
signaling processes of vascular homeostasis has changed
this view of cardiovascular calcification and redefined it asll rights reserved.
Fig. 1. The topographical and compositional information gathered from secondary electron and backscattering signals with SEM are correlated by color-coding
and overlapping, generating density-dependent color images (DDC) that highlighted the location of nano-scale calcified features within the organic matrix. The
orange color identifies denser material; structures that appear green are less dense. DDC-SEM micrographs of the aortic valve presenting (a and b) dense
spherical particles (scale bars ¼ 1 mm), (c) dense fibers (scale bar ¼ 1 mm), and (d) compact material (scale bar ¼ 10 mm).
S. Agarwal, S. Bertazzo / C. R. Chimie 19 (2016) 1605e16091606an active process [5]. This active remodeling process is
thought to involve inflammation and calcification due to
transdifferentiation of cardiovascular cells (such as vascular
smooth muscle cells and valve interstitial cells) into
osteoblast-like cells [10e12]. Although cellular disease-
driven processes can be targeted therapeutically, there
are currently no drug therapies developed specifically
against cardiovascular calcification [13]. The only treatment
today is surgery and, if the aortic or mitral valve is affected,
this means the surgical replacement of the valve. Regret-
tably, the recurrent calcification of bioprosthetic valves still
carries an operative mortality of around 50% within 10
years following surgery [4,5,14].
2.1. New perspective
Recently, materials characterization techniques have
been applied to cardiovascular calcification [15e17] in
samples of aortic valve tissue, mitral valves, coronary ar-
teries and aortas from rheumatic fever, aortic valve stenosis
and atherosclerosis patients. Scanning electron microscopy
(SEM) revealed the micro morphology of these samples,
showing that calcific lesions (the macroscopic calcific de-
posits found in diseased tissue) can include three distinct
calcified structures: spherical particles, calcified fibers and
compact calcification (Fig. 1aed).
Energy-dispersive X-ray spectroscopy (EDS) further
revealed that all three structures are composed of calcium
and phosphorus, with the spherical particles also contain-
ing magnesium (Fig. 2). The elemental composition is
therefore an indication that the different structures might
have different origins.
With regard to tissue morphology, even if the calcified
fibers in calcific lesions displayed some resemblance to thecalcified fibers in bone, spherical particles with the size re-
ported (between 100 nm and 10 microns) have never been
described in bone tissue studies. The spherical particles
reported recently were found on macroscopically visible
calcific lesions, in regions of aortic valves with no visible
calcific lesions but where calcificationwas found elsewhere
is the vascular system, and in aortic valves with no visible
calcific lesions and where the vascular system examined
was free of any calcific lesion. Unlike the calcified spheres
(Fig. 1a and b), dense fibers (Fig. 1c) and compact calcified
materials (Fig. 1d) were only identified in association with
calcific lesions and never in non-calcified tissues.
When the calcific lesions were sectioned by Focused ion
beam (FIB) and imaged by Transmission electron micro-
scopy (TEM) [18], spherical particles were found not only
on the surface of calcific lesions, but also embedded within
lesions. This is an indication that this calcification process is
not a clear-cut surface precipitation of calcium phosphate,
but rather a more complex biomineralization process that
occurs in the bulk of the tissue.
Another important piece of information provided by
electron microscopy analysis is that spherical particles are
also present inside the compact calcification. This means
that the spherical particles keep their original morphology
and internal structure while embedded in another calcified
structure, suggesting in this way that calcific lesions might
be formed by more than one process of biomineralization,
and that the growth of compact calcification structures
possibly engulfs spherical particles, which are the most
conspicuous and earliest noticeable calcified structures in
vascular tissue.
Interestingly, the internal structure of calcified spheres
was organized in rings, similarly to the internal structure of
a tree trunk. Crystallographic analyses also provided one of
Fig. 2. DDC-SEM micrographs of the aortic valve presenting dense spherical particles (a), dense fibers (b) and the compact material (c). The corresponding EDS
spectra collected at the marked () sites are indicated on micrographs aec, respectively. Scale bars ¼ 2 mm.
S. Agarwal, S. Bertazzo / C. R. Chimie 19 (2016) 1605e1609 1607the most extraordinary results, by demonstrating that the
spherical particles were formed from highly crystalline
hydroxyapatite.
The fact that these spheres can have up to 5microns and
diffract as a single crystal, makes them (to the best of our
knowledge) the most crystalline mineral present in verte-
brates. On the other hand, the compact calcification pre-
sented a poorly crystalline apatite, which is surprisingly
even less crystalline than bone mineral (Fig. 3). Once again,
the results indicate there are relevant chemical differences
between the structures of the material from calcific lesions
and bone.Fig. 3. TEM image showing spherical particles trapped in compact organic calcium
different regions of the tissue section are numbered 1e2 (scale bars ¼ 0.05 nm). S
material (1), whereas the surrounding compact material shows diffraction patternsFinally, perhaps one of the most relevant findings is that
the morphological and chemical characteristics of the
calcific material resulting in rheumatic fever, atheroscle-
rosis and aortic valve stenosis are roughly the same. This
conclusion is supported, firstly, by the finding that the
calcified material in all three diseases is formed from
calcified spherical particles, calcified fibers and compact
calcification. Moreover, samples from all different diseases
presented roughly the same morphology, the same
elemental composition and, even more strikingly, the same
crystallinity. This is particularly true for the spherical par-
ticles, which present the same internal ring-shapedphosphate matrices (scale bar ¼ 0.5 mm). The SAED patterns obtained from
pherical particles produce diffraction patterns typical of a highly crystalline
typical of a poorly crystalline material (2).
S. Agarwal, S. Bertazzo / C. R. Chimie 19 (2016) 1605e16091608structure, the same amount of magnesium in their
composition and the same electron diffraction pattern of a
single crystal across samples of tissue affected by different
calcific diseases.
Taken together, these findings provide strong evidence
that three distinct calcific diseases (rheumatic fever,
atherosclerosis and aortic valve stenosis) present a relevant
commonality in their process of calcification. In this way,
since all of them are formed by the same biomineral, they
might even present the same mechanism of biominerali-
zation. At this stage it is not possible to know if the origin of
the three diseases is the same, but it is clear that once
started, then biomineralization process produces the same
material.
Even if these results are not able to provide insights into
the biochemical or cellular mechanism by which the min-
eral is formed, they give important clues as to where
further research is more likely to discover the origin of
pathological calcification in the vascular system. The in-
formation provided urges the field to look for systems
where it is possible to produce calcium phosphate minerals
with specific morphology, composition and crystallinity.
The literature contains suggestions for the origin of
calcified material found in the tissue, such as stromal cell
microvesicles and apoptotic bodies[19]. Confirming these
hypotheses or even finding unexpected origins of these
calcified structures found in the cardiovascular system, is a
necessary step to a better understanding of calcific disease.
This knowledgewill at the same time potentially unlock the
development of new treatment and prevention methods.
3. Comparison to osteogenic theory of cardiovascular
calcification
Considering that the typical bone mineral is present
along collagen fibers, formed by poorly crystalline apatite
and composed of plate-like structures with a typical size of
20 nm [20,21] whilst calcified particles from calcific lesions
in vascular tissue are highly crystalline and with sizes
starting at 100 nm, it is clear that the material found in
vascular calcification is not bone.
Bone formation could nevertheless occur in vascular
tissue either as a concomitant event or as a consequence of
the formation of calcified particles, since themere presence
of hard spherical particles could trigger mesenchymal stem
cell differentiation to osteoblast phenotype [22,23]. It is
now well documented that in contact with practically any
tissue, calcium phosphate can lead local cells to a process of
transdifferentiation into mineralized phenotype [24e27].
Although the mechanism by which the presence of
calcium phosphate initiates the formation of a bone-like
material remains unclear, some studies provide evidence
that valve interstitial cells may contribute to or even be
responsible for the formation of calcific lesions [28].
This hypothesis might also explain why there are so
many results in the literature demonstrating the presence
of bone cells and bone proteins in calcific lesions. In this
way, the presence of these cells and proteins would indeed
indicate a correlation with bone formation, but does not
offer proof that the process of calcification is triggered by
the presence of bone cells, which could have arrived afterinitial stages of calcification, when the presence of calcium
phosphate leads to the recruitment of bone cells or differ-
entiation of vascular cells to bone cells in the calcific lesion.
4. Conclusion
To date, cardiovascular calcification has been regarded
as an actively regulated process, even though the mecha-
nisms associated with late stage mineralization remain
largely unknown. New evidence shows that vascular
calcification is not only a simple process of bone formation,
but also includes another biomineralization process that
leads to the formation of a different material hitherto un-
known. More important than just shedding light onto the
material that forms cardiovascular calcification, these new
results urge the field to look for new ways to understand
and describe vascular calcification as a process different
from osteogenic formation.
Finally, the importance of an interdisciplinary approach
to study biomedical questions such as vascular calcification
is clear. This approach provides a stepping-stone for clinical
investigation into calcific disease that will have a direct
impact on the potential development of much-needed
treatments for vascular calcification.Acknowledgments
Shweta Agarwal was supported by the British Heart
Foundation Research Excellence Award.References
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New paradigms in cardiovascular calcification

Hester Colboc

Philippe Moguelet

Vincent Frochot

Raphaël Weil

Emmanuel Letavernier

Chantal Jouanneau

Camille Francès

Claude Bachmeyer

Jean-François Bernaudin

Detection of silica and calcium carbonate deposits in granulomatous areas of skin sarcoidosis by μFourier transform infrared spectroscopy and Field Emission Scanning Electron Microscopy coupled with Energy Dispersive X-ray Spectroscopy analysis

Pierre Braunstein

C. R. Chimie 19 (2016) 1e2
lable at ScienceDirectContents lists avaiComptes Rendus Chimie
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Editorial

Ivan Huc

Jean-François Lutz

Christian Serre

C. R. Chimie 19 (2016) 17
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chemists from France? The present thematic issue, entitled
“Emerging chemistry in France”, has been put together in
order to answer these important questions. It has been
prepared in close collaboration with the Chemistry section
of the French Academy of Sciences and aims to give an
overview of a selection of promising research topics that are
currently studied in French laboratories. Thus, this issue
contains 25 articles written by leading research groups.
Importantly, the selection of these contributors was not
made at random. First of all, rather than inviting most
renowned researchers, we chose to focus on a generation of
young and confirmed talents working on expanding sub-
jects that represent the future of the field. Moreover, a wide
range of aspects of modern chemistry such as theoretical
chemistry, organic synthesis, catalysis, polymer chemistry,
supramolecular chemistry, physicochemistry, and materials
science, among others, have been included in this issue.
Hence, we hope that this thematic issue of Comptes rendus
Chimiewill give our readers a comprehensive description of
the avant-garde of French research in chemistry.
Avant-propos
Depuis plus d’un siecle, les Comptes rendus sont un reflet
de la qualite de la recherche en chimie en France. Les plus
grands chimistes français, commeMarcellin Berthelot, Henri
Moissan, Victor Grignard, Yves Chauvin et Jean-Marie Lehn,
pour n’en citer que quelques-uns, ont publie leurs travaux
dans ce journal et ont fortement contribue a son histoire.
Mais quel est l’etat des lieux en 2016 de la chimie françaisehttp://dx.doi.org/10.1016/j.crci.2016.03.001
1631-0748/© 2016 Academie des sciences. Published by Elsevier Masson SAS.
creativecommons.org/licenses/by-nc-nd/4.0/).et quels en sont les futurs leaders ? Ce numero special des
Comptes rendus Chimie, intitule « Emerging chemistry in
France », a ete specifiquement conçu pour repondre a ces
questions. Ce numero a ete prepare en etroite collaboration
avec la section de chimie de l’Academie des sciences et a
pour objectif de donner un aperçu des sujets novateurs
etudies en ce moment dans les laboratoires de recherche
français. Dans ce contexte, 25 articles de qualite sont
presentes. Il est important de preciser que la selection des
contributeurs n’a pas ete faite au hasard. Tout d’abord, nous
avons prefere faire figurer dans ce numero les travaux de
talents tres prometteurs sur des sujets en pleine expansion
plutôt que ceux de chercheurs hautement confirmes. De
plus, nous avons veille a ce qu’un vaste eventail des
thematiques de la chimie moderne, telles que la chimie
theorique, la synthese organique, la catalyse, la chimie des
polymeres, la chimie supramoleculaire, la physico-chimie et
la chimie des materiaux, entre autres, soient representes
dans ce numero. Ainsi, nous esperons que ce numero special
des Comptes rendus Chimie donnera aux lecteurs une
description realiste de l’avant-garde de la recherche fran-
çaise en chimie.
Ivan Huc
University of Bordeaux e CNRS, CBMN, UMR 5248, Institut
europeen de chimie et biologie, 2, rue Escarpit, 33600 Pessac,
France
E-mail address: i.huc@iecb.u-bordeaux.fr
Jean-François Lutz
Precision Macromolecular Chemistry, Institut Charles-Sadron,
UPR22 CNRS, 23, rue du Loess, 67034 Strasbourg, France
E-mail address: jflutz@unistra.fr
Christian Serre
Institut Lavoisier, UMR CNRS 8180, Universite de
VersailleseSaint-Quentin-en-Yvelines, 45, av. des Etats-Unis,
78035 Versailles, France
E-mail address: christian.serre@uvsq.frThis is an open access article under the CC BY-NC-ND license (http://


Emerging chemistry in France

Helena Isla

Jeanne Crassous

Helicene-based chiroptical switches

Joëlle Char

Olesia G. Kulyk

Emilie Brulé

Frédéric de Montigny

Vincent Guérineau

Thierry Roisnel

Mathieu J.-L. Tschan

Christophe M. Thomas

Microstructurally controlled polymers of <i>rac</i>-lactide by lithium complexes

Guillaume Vincent

Saloua Cheli

Rocio Martinez Mallorquin

Adi Abramovitch

Sophie Beauvière

Catherine Gomez

Franck Brebion

Ilan Marek

Max Malacria

Jean Philippe Goddard

Louis Fensterbank

Oxidation of bis-sulfinyl carbanions as the pivot of ionic/radical tandem reactions

Dayan Chlala

Madona Labaki

Jean-Marc Giraudon

Olivier Gardoll

Audrey Denicourt-Nowicki

Alain Roucoux

Jean-François Lamonier

Toluene total oxidation over Pd and Au nanoparticles supported on hydroxyapatite

Ahmed Zermane

Ouassila Larkeche

Abdeslam-Hassen Meniai

Christelle Crampon

Elisabeth Badens

Optimization of Algerian rosemary essential oil extraction yield by supercritical CO<sub>2</sub> using response surface methodology

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