Correlations among mineral components, progressive calcification

Rheumatology 2010;49:548–555
doi:10.1093/rheumatology/kep359
Advance Access publication 23 December 2009
RHEUMATOLOGY
Original article
Correlations among mineral components,
progressive calcification process and clinical
symptoms of calcific tendonitis
Hong-Jen Chiou1,2, Shih-Chieh Hung3,4,5, Shan-Yang Lin6, Yen-Shan Wei6 and
Mei-Jane Li7
Abstract
Objective. To establish the correlations among the mineral components, progressive calcification process
and clinical symptoms of calcific tendonitis.
CLINICAL
SCIENCE
Methods. The morphology of the calcified deposits on the shoulders of 28 patients with calcific tendonitis
was determined by high-resolution ultrasonography. The calcified deposit from each patient was aspirated
and determined by the Fourier transform infrared and Raman microspectroscopies. The curve-fitting
program was applied to estimate the chemical component in the calcified deposits of calcific tendonitis.
Results. The morphology of calcified deposits for 28 patients was classified into four shapes: arc shape
(7 patients), fragmented/punctuate shape (4 patients), nodular shape (13 patients) and cystic shape
(4 patients). These classified shapes markedly correlated with the pain levels in patients. The infrared
spectra of all the calcified deposits for 28 patients were easily classified into three types in the blind study
and corresponded to the formative, resting and resorptive phases in the progressive calcification process
of calcific tendonitis. With the progressive calcification, the IR wavenumber at 1018 cm1 assigned to
poorly crystalline, non-stoichiometric apatite for the formative phase was shifted to 1028 cm1 for the
resting phase and then to 1031 cm1 due to matured crystalline stoichiometric apatite for the resorptive
phase. The curve-fitted results revealed that calcified deposits in calcific tendonitis were composed of
different quantities of A-type and B-type carbonated apatites in the three phases. A significant difference
was found in carbonated apatite content among the three phases (P < 0.001).
Conclusions. The different quantities of A-type and B-type carbonated apatites determined by vibrational
microspectroscopy in calcified deposits were well correlated with those of the four shapes of morphologic
classification, with the three phases in the progressive calcification process and with the clinical symptoms of calcific tendonitis.
Key words: Calcified deposits, Calcific tendonitis, Spectral biodiagnosis, Morphology, Fourier transform infrared spectroscopy, Raman, A-type and B-type carbonated apatites, Progressive calcification, Clinical symptoms.
Introduction
1
Department of Radiology, Taipei Veterans General Hospital,
2
Department of Radiotherapy, School of Medicine, National YangMing University, 3Department of Medical Research and Education,
4
Department of Orthopaedics and Traumatology, Taipei Veterans
General Hospital, 5Institute of Clinical Medicine, School of Medicine,
National Yang-Ming University, Taipei, 6Department of Biotechnology,
Yuanpei University, Hsin-Chu and 7Department of Medical Research
and Education, Taipei Veterans General Hospital, Taipei, Taiwan,
Republic of China.
Submitted 19 May 2009; revised version accepted 1 October 2009.
Correspondence to: Shan-Yang Lin, Department of Biotechnology,
Yuanpei University, No. 306, Yuanpeu Street, Hsin Chu 30015, Taiwan,
Republic of China. E-mail: [email protected]
Calcific tendonitis of the shoulder is due to calcified
deposits located within the tendons of the rotator cuff
causing inflammation and painful symptoms [1, 2].
Although it is difficult to verify whether the pain is attributed to the tendonitis or the calcified deposits themselves,
the acute pain may occur when the calcified deposits are
undergoing resorption via phagocytosis [1, 3]. Until today,
the aetiology and pathogenesis of calcific tendonitis
remained unclear, but the calcification following metaplasia in the tendon is widely recognized [4, 5].
! The Author 2009. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: [email protected]
Different carbonated apatites in calcified deposits
Uhthoff et al. [4, 6] had proposed a cyclically evolutionary calcification process for calcific tendonitis:
pre-calcification stage ! calcification stage ! postcalcification stage. The second calcification stage in this
cyclic process might also be subdivided into formative,
resting and resorption phases. These three phases were
induced by the active mediation of calcification due to
cells in a viable condition, and caused shoulder pain [6–
8]. According to the time-dependent pain symptom and
time-associated calcification progression, we have
proposed and reconstructed an evolutionary model of
the progressive calcification process and clinical symptoms of calcific tendonitis of the shoulder, as shown in
Fig. 1 [4, 9]. The diagnosis of this disease is based
on clinical examination by using a variety of imaging techniques [9–11]; however, it may be markedly influenced by
the experience of the radiologist and instruments used.
The existing classification and diagnosis based on radiographs showed different consistency and reliability. It will
be interesting to see whether there is a correlation
between the extent of calcification and clinical symptoms
in these three phases.
It has been reported that chronic or acute calcific
tendonitis was predominantly caused by the deposition
of hydroxyapatite (HAP) in the periarticular tendon, but
no significant differences were found in the symptoms of
either type [8]. An inflammatory reaction might be
FIG. 1 The proposed evolutionary model of the
progressive calcification and clinical symptoms of calcific
tendonitis of the shoulder.
triggered by these HAP crystals through the up-regulation
of inflammation mediators. The inflammatory potential of
HAP crystals has been reported to vary according to
crystal features, such as specific surface area, size and
density of the crystals, as well as the calcium/phosphate
ratio. The physicochemical heterogeneity of crystals might
also be an additional factor leading to inflammation
[12, 13]. The carbonate ion (CO2
3 ) is known to occupy
two different positions in the crystal lattice of HAP
[Ca10(PO4)6(OH)2]. It can substitute for the OH site
(defined as A-type carbonated apatite) or for the PO3
4
site (defined as B-type carbonated apatite), in which the
B-type carbonated apatite is the major mineral species
of the biological apatites [14, 15]. Whether the crystal
features of the carbonated apatite may affect the inflammatory properties and clinical symptoms is unknown.
Although the carbonated apatite has been reported to
be a single component in the calcified deposits of calcific
tendonitis [2, 8, 16], there are no investigations concerning
the role of the types of carbonated apatites in calcific
tendonitis.
Recently, the use of vibrational spectroscopy has
shown great potential over other diagnostic techniques
to successfully investigate the chemical composition of
the diseased tissue, rather than histological pathology
alone [17, 18]. The Fourier transform infrared (FT-IR) and
Raman spectroscopies provide similar but complementary information on molecular–structural fingerprints of
the samples. Both techniques are suitable to analyse the
mineral structure with fast and non-destructive analysis,
since they are also sensitive to the changes in crystallinity
or molecular substitution. They can directly determine the
tiny samples via the microscope system without special
sample preparation. In our previous studies, several
human calcified tissues, such as calcinosis cutis, skin
pilomatrixoma, cornea, senile cataractous lens, vitreous
asteroid bodies and sclera, had been investigated by
using these vibrational microspectroscopic techniques
[18, 19]. The purpose of this study was to quantitatively
determine the type and content of chemical components
in the calcified deposits of calcific tendonitis by FT-IR and
Raman microspectroscopies. Moreover, the correlations
of the mineral composition in calcified deposits with
progressive calcification process or with clinical courses
and symptoms of calcific tendonitis were also explored.
Patients and methods
Patients
The outer circle exhibits the evolutionary process of calcification stages for calcific tendonitis. The middle circle
looks at the active mediation of calcification by cell in a
viable condition. The inner circle indicates the cellular
response and clinical symptoms (adapted and modified
from Uhthoff and Loehr [4] and Sherman and Marx [9]).
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Twenty-eight patients with shoulder pain due to calcific
tendonitis were enrolled in this study [11 men and
17 women; age range 46–81 (average 57) years]. All
patients were referred from the outpatient department
of Orthopaedics. The enrolled criteria in patients included
chronic shoulder pain for at least 6 months with or without
acute exacerbation. Diagnostic high-resolution ultrasonography (HRUS) was carried out initially to verify the calcific
tendonitis. The HRUS with a GE Voluson E8 system (GE
Medical Systems, Milwaukee, WI, USA) using S10-16-D
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Hong-Jen Chiou et al.
linear probe and Philips IU22 system, and HDI 5000 using
L12-5 linear probe (Philips-ATL, Bothell, WA, USA) were
used for imaging measurements. Each patient was
explained the procedure very clearly and signed the
consent form before the procedure. The present study
was approved by the Institutional Review Board at the
Taipei Veterans General Hospital according to the
Declaration of Helsinki.
Clinical evaluation method
All patients had undergone an HRUS examination and
showed a calcific tendonitis. The clinical symptoms were
modified from the visual analogue scale (VAS) system,
and patient symptoms were graded as painless (0), mild
(1–4), moderate (4–8) and severe (8–10), according to the
patient’s chief complaint and the compression of a probe
to the calcified deposits [5, 20, 21]. There were 10 patients
with mild shoulder pain, 8 patients with moderate-degree
shoulder pain and 10 patients with severe shoulder pain in
this study. The morphology of the calcified deposit of the
shoulder determined by HRUS was classified into four
shapes: arc (an echogenic arc with clear shadowing,
Fig. 2A); fragmented or punctuate (at least two separated
echogenic spots or plaques with or without shadowing,
Fig. 2B); nodular (an echogenic nodule without shadowing, Fig. 2C); and cystic (a bold echogenic wall with an
anechoic area, weak internal echoes or layering content,
Fig. 2D).
Aspiration method
The ultrasound-guided puncture was repeatedly undertaken for each patient, according to our previous
method [5, 20, 21]. In the puncture procedure, which
was performed with the free-hand method monitored
with HRUS, the needle tip was placed in the calcified
plaque, which was then punctured by moving the needle
back and forth with 2-ml negative pressure aspirated.
After the procedure, the puncture site was bandaged
with hand compression for 15 min by the patient himself
who was then sent back home without any complications.
The calcified deposit was aspirated into two parts for histopathological examination and vibrational microspectroscopic study.
Histopathological examination
Each calcified deposit was processed routinely to
produce 5-mm paraffin-embedded tissue sections and
stained with haematoxylin and eosin (H&E). The sample
FIG. 2 The representative sonogram of each calcified deposit of the shoulder examined by HRUS.
(A) An arc-shape calcification (arrows) was found over the supraspinatus tendon in a 48-year-old female who complained
of right-shoulder pain for >6 months. (B) A punctuate calcification (arrows) was observed in the right supraspinatus
tendon in a 46-year-old female who complained of right-shoulder pain for 1 year. (C) A fragmented nodular type calcification (arrows) in right shoulder was found in a 53-year-old female patient who complained of chronic shoulder pain for
>1 year. (D) A cystic type (arrows) with bold echogenic rim on the left subscapularis tendon was observed in a 53-yearold female patient who complained of chronic pain over the left shoulder for >2 years.
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Different carbonated apatites in calcified deposits
was observed by using the light microscopy (BH-2,
Olympus, Tokyo, Japan).
the existence of a calcified deposition [22]. Figure 2 shows
the representative sonogram of each calcified deposit of
the shoulder examined by HRUS, in which the arrows
indicate the shape of calcification. It clearly indicates
that the HRUS could easily classify the calcified deposits
into four shapes including the arc (Fig. 2A), fragmented/
punctuate (Fig. 2B), nodular (Fig. 2C) and cystic (Fig. 2D).
In the present study, the morphology of the calcified
deposits may be classified into an arc shape in 7 patients
with clinical symptoms (6 mild and 1 moderate),
fragmented/punctuate shape in 4 patients (3 mild and
1 severe), nodular shape in 13 patients (1 mild, 6 moderate
and 6 severe) and cystic shape in 4 patients (1 moderate
and 3 severe), as shown in Table 1. That is, there were
16 out of 18 patients with moderate to severe clinical
symptoms occurring in nodular or cystic type calcification.
Obviously, there was a positive correlation between the
morphology of the calcified deposits and the clinical
symptoms of the shoulder pain with significant difference.
All the infrared (IR) spectra of calcified deposits for the
28 patients with calcific tendonitis can be clearly classified
into three types in the blind study, as shown in Fig. 3A-a, b
and c. The IR spectrum of HAP reference standard is also
displayed (Fig. 3A-d). It is surprising to note that each type
of IR spectrum was exactly attributed to that of the above
morphologic classification. The representative IR spectrum in Fig. 3A-a might refer to the IR spectrum of calcified
deposits for the arc and fragmented/punctuate types. The
representative IR spectrum in Fig. 3A-b or -c belonged to
the IR spectrum of calcified deposits for the nodular or
cystic type, respectively. According to the timedependent fate of calcified deposits in Fig. 1, these
three types of IR spectra may be defined as the results
of formative, resting and resorptive phases in the calcification stage of progressive calcification process of calcific tendonitis (Table 1).
These three types of IR spectra were also closely similar
to each other in many positions of the wavenumber,
except the predominant IR peaks 1018–1031/cm
assigned to the 3 stretching vibration of phosphate for
the apatite structure [17, 18, 23]. The IR peaks at 872–
875, 1413–1416 and 1451–1455/cm were due to the IR
wavenumbers of 2 stretching mode of carbonate bands
in these calcified samples, but the IR peak at 959–961/cm
corresponded to the 1 symmetric stretching phosphate.
The IR spectrum of HAP indicates several characteristic
Vibrational microspectroscopic study
The blind study was initially performed and the code name
was only given for spectral analysis. The sample of calcified deposit was washed with distilled water and centrifuged. The process was carried out twice. The sample
was then dried for 1 day at 25 C, 50% relative humidity
conditions. The dried samples were directly examined to
identify and determine the chemical component by using
both FT-IR microspectroscopy (Micro FTIR-200; Jasco
Co, Tokyo, Japan) with a transmission technique and confocal micro-Raman spectrophotometer (Jasco Ventuno,
Jasco Co., Tokyo, Japan) equipped with a 30-mW green
(532 nm) solid-state laser standard via non-destructive
analysis [18, 19]. The IR spectra were carried out at 200
scans and a resolution of 4/cm, but the pixel resolution of
Raman system was 1.3/cm. Synthetic HAP (>100 mesh;
purity, >99.5%; Nacalai Tesque, Tokyo, Japan) was used
as a standard reference.
Spectral data acquisition and handling
(1) Spectral analysis. A spectra manager (Jasco Co.,
Tokyo, Japan) and GRAMS spectroscopy software suite
(Thermo Electron Co., Waltham, MA, USA) were used for
spectral data processing. Second-derivative FT-IR spectral analysis was applied to locate the position of the overlapping components of samples.
(2) Compositional component determined by curve-fitting
program. The IR spectral ranges within 888 and 862/cm
were quantitatively estimated by the curve-fitting
algorithm using the Gaussian function with the minimum
standard error. The composition of each component was
computed to be the fractional area of the corresponding
peak, divided by the sum of the areas of all the peaks.
(3) Statistical analysis. For comparisons of these variables, analysis of variance (ANOVA) was used. All results
were expressed as the mean (S.D.). P-values <0.05 were
considered to be of significant difference.
Results
The histopathological examination of the sliced sample
revealed a deep blue–purple on the H&E stain, implying
TABLE 1 Correlations among the shapes of calcified deposits, clinical symptoms and calcification stages proposed
Clinical symptoms
Morphologic shape
Patient no.
Arc
Fragmented/punctuate
Nodular
Cystic
7
4
13
4
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Painless
0
0
0
0
Mild
Moderate
6
3
1
0
1
0
6
1
Severe
0
1
6
3
Calcific stage proposed
Formative phase
Formative phase
Resting phase
Resorptive phase
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Hong-Jen Chiou et al.
FIG. 3 The representative IR and Raman spectra of calcified deposits for different morphological classifications of
patients with calcific tendonitis.
(A) Arc and fragmented/punctuate shapes, also corresponding to the formative phase in the calcification stage of progressive calcification process. (B) Nodular shape, also corresponding to the resting phase in the calcification stage of
progressive calcification process. (C) Cystic shape, also corresponding to the resorptive phase in the calcification stage
of progressive calcification process. (D) HAP reference standard.
absorption peaks at 875, 961, 1031, 1090 and 3569/cm, in
which the peaks at 961, 1031 and 1090/cm corresponded
to the stretching modes of phosphate but at 875/cm
attributed to carbonate ions. A unique peak positioned
at 3569/cm was due to the OH-group of HAP. In the fingerprint region of 900–1200/cm, a predominant peak at
1018/cm for calcified deposits of formative phase was
gradually shifted to 1031/cm with the progressive calcification process and it was close to that of the IR spectrum
of HAP. This clearly indicates that apatite was a key component in the calcified deposits of calcific tendonitis.
Moreover, the amide I and II bands of protein at 1643–
1654 and 1541–1545/cm were also observed in the IR
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spectra of these calcified deposits. The 2800–3000/cm
spectral region attributed to the CH2 and CH3 stretching
vibrations of protein was also found. This reveals that
some proteins had adhered to the calcified sample [17,
18, 23].
On the other hand, there was no significant difference
among Raman spectra in the three phases, as displayed
in Fig. 3B. Several small peaks at 2800–3000, 1665–1667
and 1449–1452/cm corresponding to the protein structure
and a peak at 1000–1004/cm assigned to HPO
4 and/or
phenylalanine were obtained in the Raman spectra of the
three phases. A predominant peak at 958–961/cm and a
small peak at 1071–1072/cm were found in these Raman
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Different carbonated apatites in calcified deposits
spectra, which were due to the 1 stretching mode of
phosphate and carbonate, respectively [17, 18, 24]. The
typical Raman spectrum of HAP was normally found at
961 and 1045/cm due to 1 and 3 stretching vibration
of phosphate. A unique peak at 3576/cm due to the OH
group was also observed in the Raman spectrum of HAP.
The OH band at 3569/cm in IR spectrum and at 3576/cm
in Raman spectrum was absent from all the IR and Raman
spectra, which implies complete occupation of the OH
sites of HAP by carbonate in all calcified samples [8].
Discussion
It is well known that crystal deposition is also a type of
biomineralization process causing many disorders and
symptoms in different human organs [25, 26]. Although
calcific tendonitis of the rotator cuff is one of the crystal
deposition disorders and is also characterized by an
inflammation around the HAP crystal deposits, the
progressive calcification process and clinical symptoms
of calcific tendonitis remain unclear. In this study, the
morphology of calcified deposits was variable from arc
type to cystic type. Table 1 indicates that with the
exacerbation of calcification from arc to cystic, the clinical
symptoms were more serious, from mild to severe, suggesting that the morphology of calcified deposits was well
correlated with the clinical symptoms of calcific tendonitis. The result was similar to our previous study [5, 20, 21].
Furthermore, the changes in morphology were also correlated with the fate of calcified deposits from mineralization, enlargement and liquefaction, and phagocytosis by
accompanying clinical symptoms of shoulder pain (Fig. 1).
According to the histology, there are three recognized
stages of calcific tendinitis including the pre-calcification,
calcification and post-calcification stages [4, 7]. Since
most patients are asymptomatic during the precalcification phase, the calcification stage subdivided
into the formative, resting and resorptive phases should
be the main clinical symptom on which to base a diagnosis and give treatment in hospital. However, the intact
constitution of calcified deposits in each type is unknown.
Understanding the exact composition of calcified deposition at each phase and stage in calcific tendonitis is of
great importance in a variety of pathological diagnosis.
In the spectral analysis of the mineralization process,
two IR spectral regions at 900–1200/cm (1 and 3 stretching modes of phosphates) and 860–890/cm (2 stretching
mode of carbonate) of mineralized materials had recently
been used for FT-IR spectroscopic examination [17, 18,
27]. It has been reported that a peak near 1020/cm is
attributed to the 3 vibration of PO3
4 in poorly crystalline,
non-stoichiometric apatites, but a peak at 1030/cm is
indicative of the 3 vibration of PO3
4 in matured crystalline
stoichiometric apatites [27, 28]. Thus, the crystallinity and
maturity of biological apatites can be estimated by the
peak intensity or peak area ratio of 1020/1030/cm. With
maturation, apatitic lattice may evolve towards a greater
order leading to the decrease in the ratio value of 1020/
1030/cm. Here, the HAP sample used in this study
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exhibited a unique peak at 1031/cm, indicating that it
belonged to a matured crystalline stoichiometric apatite.
As shown in Fig. 3A, a sample of the formative phase
showed a predominant IR peak at 1018/cm, suggesting
that the calcified deposits of calcific tendonitis at
this phase consisted of the poorly crystalline, nonstoichiometric apatites [27, 28]. With the progressive
calcification process of calcific tendonitis, the wavenumber of this unique peak shifted from 1018/cm (formative
phase) to 1028/cm (resting phase) and then to 1031/cm
(resorptive phase). The calcified deposits of the resorptive
phase seemed to be close to the matured crystalline
stoichiometric apatite of HAP used. The maturation of
apatite from the poorly crystalline, non-stoichiometric
state at the early stage to the matured crystalline stoichiometric state at the later stage was associated with the
progressive calcification of calcific tendonitis, indicating
that mineralization progressively occurred in the calcified
deposits of calcific tendonitis.
FT-IR vibrational spectroscopy has also been applied to
determine the location of the carbonate ions in biological
minerals [14, 15, 17, 18]. Carbonate is one of the substituting ions; it may substitute for either the OH (A-type
carbonated apatite) or PO3
4 (B-type carbonated apatite)
anions in the crystal lattice of apatites or it may be in
unstable locations. IR spectroscopic results of the fully
mineralized samples have shown that the carbonate
domain region have three combands in the 2 CO2
3
ponents: the major component near 871/cm is due to
the B-type carbonate; a band near 878/cm is assigned
to the A-type carbonate; and a band 866/cm is due to
the liable carbonate ions located in the poorly crystalline
environments and not incorporated into the apatitic lattice
[14, 15]. With the increase of maturation, the 866/cm
shoulder intensity decreases as compared with the
871/cm intensity.
In this study, the typical spectral region of 2 stretching
and the three underlying bands are
mode of CO2
3
deduced by a curved-fitting analysis, as shown in Fig. 4.
Obviously, three components were included in the
spectral region of 862–888/cm. The assignment and
composition of the curve-fitted original IR spectrum of
HAP were obtained as follows: 882/cm (15.1%), 875/cm
(65.1%) and 868/cm (19.8%). Three components of each
calcified deposit for 28 patients are revealed in Fig. 5.
All data were close to each other and the differences in
variability between the same groups were minimized.
The mean (S.D.) values of each component in different
phases are also shown in Fig. 5. Statistical analysis
indicates that significant differences were observed
among the three phases: formative phase and resting
phase (P < 0.001); formative phase and resorptive phase
(P < 0.01–0.001); resting phase and resorptive phase
(P < 0.001) except the liable carbonate ions (P > 0.05).
It strongly indicates that the IR spectral region of 862–
888/cm for carbonate was a useful range for differentiating the progressive calcification process. Moreover, the
classification of three phases in the progressive
calcification process of calcific tendonitis was validated.
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Hong-Jen Chiou et al.
FIG. 4 (a–d) The assignment and composition of the
curve-fitted original infrared spectrum of the calcified
deposits for different morphological classifications of
patients with calcific tendonitis (Fig. 3).
FIG. 5 The variability of curve-fitted three compositions of
calcified deposits in the same or different morphological
classifications or calcification stages after FT-IR
microspectroscopic determinations.
reveals that carbonate ions located in the liable sites
were lost during the maturation process. Moreover, a
slight decrease of those located in the A-type position
and an increase of those located in the B-type site is
also indicated in Fig. 5. The result strongly supports that
the maturation of mineral fractions in calcified tissues of
calcific tendonitis also gradually proceeds in the progressive calcification process.
There are three limitations in the present study. First,
the specimens of calcified deposits were sampled from
the rotator cuff. Secondly, the cases of resorptive phase
in the progressive calcification process were less than
other phases, since some calcified deposits were gradually resorbed into the body leading to the lack of sampling.
Thirdly, the change in the composition of the calcified
deposits in the same patient was not available in the present study because the patient refused the puncture again
in a short time. Further studies are needed to investigate
the composition of calcified deposit in ineffective
repeated punctures of calcific tendonitis.
In conclusion, the result of the present study indicates
that different quantities of A- and B-type carbonated apatites in calcified deposits are reflected in the formative,
resting and resorption phases in the calcification stage
of the progressive calcification process of calcific tendonitis. Reduced amounts of carbonates located in the liable
and in A positions but increased amounts located in B
positions were found in this progressive calcification process. Moreover, these three phases in the calcification
stage of the progressive calcification process were well
correlated with the morphology of calcified deposits and
clinical symptoms of shoulder pain for calcific tendonitis.
Correlations among the mineral components, progressive
calcification process and clinical symptoms of calcific
tendonitis were established.
Rheumatology key messages
Vibrational spectroscopy effectively evaluated the
types and contents of carbonated apatites in the
calcified deposits.
. Carbonated apatites located in the liable and
A positions were reduced but increased in the
B positions.
. Compositional changes in the calcified deposits
were well correlated with morphology, progressive
calcification process and clinical symptoms.
.
Acknowledgement
Dotted line indicates the mean value of composition.
Since the composition of the 866/cm band was
reduced with the progressive calcification process, the
mineralization in calcified deposits of calcific tendonitis
has gradually grown towards the maturation. It clearly
554
The authors would like to thank the patients for their
contribution.
Funding: This work was supported by a grant of National
Science Council, Taipei, Taiwan, Republic of China
(NSC-97–2320-B075–054-MY3).
Disclosure statement: The authors have declared no
conflicts of interest.
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Different carbonated apatites in calcified deposits
1 Hurt G, Baker CL Jr. Calcific tendinitis of the shoulder.
Orthop Clin North Am 2003;34:567–75.
15 Sønju Clasen AB, Ruyter IE. Quantitative determination of
type A and type B carbonate in human deciduous and
permanent enamel by means of Fourier transform infrared
spectrometry. Adv Dent Res 1997;11:523–7.
2 Garcia GM, McCord GC, Kumar R. Hydroxyapatite crystal
deposition disease. Semin Musculoskelet Radiol 2003;7:
187–93.
16 Hamada J, Ono W, Tamai K, Saotome K, Hoshino T.
Analysis of calcium deposits in calcific periarthritis.
J Rheumatol 2001;28:809–13.
3 Doumas C, Vazirani RM, Clifford PD, Owens P. Acute
calcific periarthritis of the hand and wrist: a series and
review of the literature. Emerg Radiol 2007;14:199–203.
17 Mantsch HH, Choo-Smith LP, Shaw RA. Vibrational
spectroscopy and medicine: an alliance in the making.
Vib Spectrosc 2000;30: 31–41.
4 Uhthoff HK, Loehr JW. Calcific tendinopathy of the rotator
cuff: pathogenesis, diagnosis, and management. J Am
Acad Orthop Surg 1997;5:183–91.
18 Lin SY, Li MJ, Cheng WT. FT-IR and Raman vibrational
microspectroscopies used for spectral biodiagnosis of
human tissues. Spectroscopy 2007;21:1–30.
5 Chiou HJ, Chou YH, Wu JJ, Hsu CC, Huang DY,
Chang CY. Evaluation of calcific tendonitis of the rotator
cuff: role of color Doppler ultrasonography. J Ultrasound
Med 2002;21:289–97.
19 Chen KH, Li MJ, Cheng WT, Balic-Zunic T, Lin SY.
Identification of monoclinic calcium pyrophosphate
dihydrate and hydroxyapatite in human sclera using
Raman microspectroscopy. Int J Exp Pathol 2009;90:
74–8.
References
6 Uhthoff HK, Sarkar K, Maynard JA. Calcifying tendinitis: a
new concept of its pathogenesis. Clin Orthop Relat Res
1976;118:164–8.
7 Uhthoff HK, Dervin GF, Loehr JF. Calcifying tendinitis.
In: Rockwood CA Jr, Matsen FA, eds The shoulder.
3rd edition. Philadelphia: Saunders, 2004:1033–58.
8 Hamada J, Tamai K, Ono W, Saotome K. Does the nature
of deposited basic calcium phosphate crystals determine
clinical course in calcific periarthritis of the shoulder?
J Rheumatol 2006;33:326–32.
9 Sherman SL, Marx RG. Calcific tendinitis. In: Galatz LM,
ed. Orthopaedic knowledge update: shoulder and elbow
3. Illinois: American Academy of Orthopaedic Surgeons,
2008:569–75.
10 Shahabpour M, Kichouh M, Laridon E, Gielen JL, De
Mey J. The effectiveness of diagnostic imaging methods
for the assessment of soft tissue and articular disorders of
the shoulder and elbow. Eur J Radiol 2008;65:194–200.
11 Collins R, Cranny G, Burch J et al. A systematic review of
duplex ultrasound, magnetic resonance angiography and
computed tomography angiography for the diagnosis and
assessment of symptomatic, lower limb peripheral arterial
disease. Health Technol Assess 2007;11:1–184, iii–iv, xi–
xiii.
12 Prudhommeaux F, Schiltz C, Lioté F et al. Variation in the
inflammatory properties of basic calcium phosphate
crystals according to crystal type. Arthritis Rheum 1996;
39:1319–26.
13 Boskey AL, Bullough PG, Vigorita V, Di Carlo E. Calciumacidic phospholipid-phosphate complexes in human
hydroxyapatite-containing pathologic deposits. Am J
Pathol 1988;133:22–9.
14 Penel G, Leroy G, Rey C, Bres E. Micro Raman spectral
study of the PO4 and CO3 vibrational modes in synthetic
and biological apatites. Calcif Tissue Int 1998;63:475–81.
www.rheumatology.oxfordjournals.org
20 Pan PJ, Chou CL, Chiou HJ, Ma HL, Lee HC, Chan RC.
Extracorporeal shock wave therapy for chronic calcific
tendinitis of the shoulders: a functional and sonographic
study. Arch Phys Med Rehabil 2003;84:988–93.
21 Chiou HJ, Chou YH, Wu JJ et al. The role of highresolution ultrasonography in management of calcific
tendonitis of the rotator cuff. Ultrasound Med Biol 2001;
27:735–43.
22 Sundaram S, Kuruvilla S, Thirupuram S. Idiopathic arterial
calcification of infancy—a case report. Images Paediatr
Cardiol 2004;18:6–12.
23 Gourion-Arsiquaud S, West PA, Boskey AL. Fourier
transform-infrared microspectroscopy and microscopic
imaging. Methods Mol Biol 2008;455:293–303.
24 Antonakos A, Liarokapis E, Leventouri T. Micro-Raman
and FTIR studies of synthetic and natural apatites.
Biomaterials 2007;28:3043–54.
25 Kirsch T. Determinants of pathologic mineralization.
Crit Rev Eukaryot Gene Expr 2008;18:1–9.
26 Swift JA. Biomineralization of organic phases associated
with human diseases. In: Novoa JJ, Braga D, Addadi L,
eds Engineering of crystalline materials properties.
Dordrecht: The Netherlands: Springer, 2008:449–75.
27 Carden A, Morris MD. Application of vibrational
spectroscopy to the study of mineralized tissues (review).
J Biomed Opt 2000;5:259–68.
28 Rey C, Shimizu M, Collins B, Glimcher MJ. Resolutionenhanced Fourier transform infrared spectroscopy
study of the environment of phosphate ion in the early
deposits of a solid phase of calcium phosphate in
bone and enamel and their evolution with age: 2.
Investigations in the nu3PO4 domain. Calcif Tissue Int
1991;49:383–8.
555