Original papers
DOI: 10.11152/mu.2013.2066.172.mcphAbstract
Aim: To evaluate the metacarpophalangeal (MCP) joints (MCP2 and 5) in healthy subjects by ultrasonography (US) using a high frequency transducer (18 MHz) and to verify the interobserver agreement. Material and methods: We enrolled 50 healthy volunteers (37 women, age between 30-58 years, mean age 41.7 years, divided into 3 groups according to age: 30-39, 40-49, and 50-58 years). The subjects were successively evaluated by 4 rheumatologists: 2 experienced (team A) and 2 beginners (team B) in US. Seven dorsal and palmar longitudinal scanning positions and a supplementary scan for MCP cartilage were performed.
The bone surface (erosions, osteophytes), the intra-articular content (synovial thickening and vascularization, 4 grade scale), and the aspect of the metacarpal head cartilage were analyzed. The anterior palmar recess was measured. The time for examination was recorded. Results: Erosions were detected in 7% of joints by team A and 2% by team B (p<0.05, kappa agreement 0.567) in subjects over 40 years. The agreement by team A in the detection of the erosions was very good (kappa value 0.83). A moderate positive correlation was obtained between the presence of erosions and age (r= 0.401, p=0.004). Osteophytes were identified only on the dorsal scan in subjects over 50 years (in 3.5% of joints team A, 1.5% team B, p>0.05, kappa value 0.421). No grade 1 synovitis was observed by team A but 4 joints with grade 1 synovitis were identified by team B (p<0.05) from the dorsal scan.
The dimensions of the palmar recess had large distribution (MCP 2 between 0.55-1.3 mm; MCP 5 between 0.6-1.2 mm). No statistical significant differences were obtained when comparing the dimensions of the two hands or the values obtained in age- groups (all p>0.05). No statistical significant correlations were obtained between the dimensions of palmar recess and the body mass index or dominant hand (all p>0.05). No pathological findings were found in the examination of the metacarpal head car- tilage. Power Doppler investigation found the presence of grade 1 signal in 2.5% joints by team A and 1.5% by team B (p>0.05) only in the dorsal scans. The mean time for examination was 7.8±1.74 min in team A and 13.78±2.96 min in team B (p<0.05).
Conclusions: In healthy subjects pathological findings are occasionally encountered, especially erosions and osteophytes. Us- ing an 18 MHz transducer the aspect of grade 1 synovitis was not encountered in healthy non-inflammatory MCP joints. There is a permanent need for standardized training and examination in musculoskeletal US.
Keywords: ultrasonography, high frequency transducer, metacarpophalangeal joints, healthy subjects
Ultrasonography of the metacarpophalangeal joints in healthy subjects using an 18 MHz transducer.
Daniela Fodor
1, Ioana Felea², Daniela Popescu
3, Adelina Moţei
3, Paula Ene
1, Oana Şerban
1, Mihaela Micu
412nd Internal Medicine Department, “Iuliu Hatieganu” University of Medicine and Pharmacy, Cluj-Napoca, 2Rheu- matology Department, Emergency Clinical County Hospital, Cluj-Napoca, 3Rheumatology Department, University of Medicine and Pharmacy, Cluj-Napoca, 4Rheumatology Division, Department of Rehabilitation II, Rehabilitation Clinical Hospital,Cluj- Napoca, Romania
Received 20.03.2015 Accepted 26.04.2015 Med Ultrason
2015, Vol. 17, No 2, 185-191
Corresponding author: Daniela Fodor, MD, PhD 2nd Internal Medicine Department
“Iuliu Hatieganu” University of Medicine and Pharmacy, Cluj-Napoca, Romania 2-4 Clinicilor str, 400006 ClujNapoca, Romania Phone: 004 0264591942/442
Email: [email protected]
Ultrasonography (US) has become in the latter years
an essential tool in rheumatological practice for diagno- sis, monitoring, and assessment of remission in all patho- logical situations that involve the joints and/or periarticu- lar structures [1]. Due to the increased quality of the US machines and, more important, of the higher frequency of the transducers used for the evaluation of the small joints, it is now possible to identify lesions/structures smaller than 1 mm. It is well known and accepted that US is more sensitive and reliable compared with clinical examination, not only for the small joints but also for the large joints [2-4]. That is why it is mandatory to clearly delimitate the normal from pathologic US findings, to
recognize anatomical variants, to identify physiological situations, and to understand the anatomy and histology of the joints.
Being considered an operator-dependent tool, stand- ardization of the US was a matter of debate over the years.
In 2005 OMERACT (Outcome Measures in Rheumatoid Arthritis Clinical Trials) group published an expert con- sensus on US definitions for pathological findings in in- flammatory rheumatologic diseases [5]. These definitions are considered to form a standardized nomenclature.
Grey-scale US is well suited for synovium visualiza- tion. The scoring systems developed for grading the syn- ovial hypertrophy generally used semiquantitative crite- ria [6-8], being considered to be the standard approach.
The Szkudlarek et al scoring system [8] is the most used for scientific and clinical purpose. In all the scoring sys- tems the appreciation of the grade in synovium prolif- eration (considered to be hypoechoic/anechoic) is made by comparing the level of intra-articular hypoechoic/an- echoic structures with the bone landmarks (periarticular bones contour). The difference between the joint fluid and proliferated synovium was taken into consideration in Scheel et al [7] and Szkudlarek et al [8] scores but not in the Backhaus et al [6] score. In fact, in practice this difference is frequently difficult to be assessed; even in the OMERACT definition it is stated that synovial fluid can be hypoechoic or anechoic and synovial hypertrophy hypoechoic (but sometimes isoechoic or hyperechoic).
The displacement/compression with the transducer of the intra-articular hypo/anechoic structure may contribute to establish the difference. For these reasons the term of
“synovitis” should be reserved only for cases with proved inflammation by using color/power Doppler [9]. The cor- rect interpretation of the grade 1 grey-scale US aspect of the MCP (normal or minimal synovial thickening) is one of the most debated subjects [9-12] concerning US criteria for early inflammatory arthritis.
The anatomy of the metacarpophalangeal (MCP) joint is complex (fig 1). During the time numerous anatomic and imaging (US, magnetic resonance imaging) studies were performed in order to describe all the structures in- volved in the functionality of this joint [9,13-17] and to explain the localization of the lesions in specific parts of the joints [17]. The US appearance of normal MCP joint is largely influenced by the examination techniques: the perpendicular examination in order to avoid anisotropy, the correct setting for grey-scale of the US machine, the use of high frequency transducers, the quantity of gel (transducer not in contact with the skin), the joint posi- tion [18], the quality of images acquisition, etc. The ma- jority of US studies were performed using transducers with frequency lower than 18 MHz. Higher frequencies
produce better resolution (but lesser penetration) and in- vestigating this superficial joint with 18 MHz transducer could bring new data regarding its normal appearance.
The aims of our study were to evaluate the MCP joints (the second and the fifth MCP) in healthy subjects by US using a high frequency transducer (18 MHz), to establish the frequency and localization of inflammatory (hypertrophied synovium and PD signal) and chronic (erosions and osteophytes) lesions. Also, we intended to measure the required time for evaluation and to verify the interobserver agreement (between experienced and un- experienced examiners) of the findings.
Material and methods
In this prospective study 50 healthy volunteers (37 women, age between 30-58 years, mean age 41.7 years) from the medical staff of our hospital were enrolled.
The subjects were enrolled if they have/had no history of pain, arthritis, trauma, or surgery of the fingers joints and if the clinical examinations (performed by an experi- enced rheumatologist) of the joints was in normal range.
Data about age, weight, height, body mass index (BMI) calculated as weight/height2 and expressed in kg/m2, physical and sport activities (mild, moderate, intense), and dominant hand were collected. Written, informed consent for participation was obtained from each subject prior to enrolment. The Ethics Committee of the Univer- sity approved the study protocol.
The subjects were successively evaluated by 4 rheu- matologists: 2 with high experience in musculoskeletal US (team A, with 16 and 8 years of experience) and 2 with minimum experience (4 hours training in US ex- Fig 2. Anatomical drawing of the metacarpophalangeal joint: a) longitudinal aspect; b) transversal aspect at level of the proximal phalanx base. MC – metacarpal bone, PP – proximal phalanx, E – extensor tendon, F – flexor tendons (superficial and pro- found) in the synovial sheath, L – lumbrical tendon, I – interos- seous tendon, S – sagittal band, MCL – main collateral ligament, ACL – accessory collateral ligament, DLT – deep transverse metacarpal ligament, black arrow – dorsal plate, white arrow- palmar (volar) plate.
amination of the MCF) in US (team B). All the exami- nations were blinded concerning the results of the other investigators. The US examinations were performed be- tween 9-11 a.m., after 30 min of relative rest of the hands, without heavy physical work/exercises in the previous 24 hours of examination, and in the same conditions of tem- perature or light.
A standard scanning protocol was used in every sub- ject. The patient was examined in sitting position, with both hands placed on a table in extension position with the EsaoteMyLab 50 machine using 18 MHz transducer.
The larger depth of the machine (2 cm), two focuses, and intermediary time gain control (TGC) were used for grey- scale US. Power Doppler (PD) was assessed using the highest gain level without background noise and pulse repetition frequency of 750 MHz. A sufficient quantity of gel was used in every case (the transducer has not to be in contact with the skin). The scanning protocol was derived from the work of Ellegaard et al [9]. We chose to investigate MCP 2 and 5 as these joints are the most ac- cessible MCF joints for US investigations.
The second and fifth MCPs of both hands were as- sessed with US in seven dorsal and palmar longitudinal scanning positions and a supplementary scan for MCP cartilage (50 subjects, 200 joints, 1600 US scanning po- sitions) (details for MCF 2 examination in figure 2; for MCF 5 the radial side was inversed by the ulnar side).The following aspects were recorded: bone surface (smooth or with irregularities: erosions- step down irregularities visible in two perpendicular plans, osteophytes- step up irregularities) and the intra-articular content- synovial thickening (4 grade semiquantitative score [8]) and vas- cularization (4 grade scale [6]) from all the scanning po- sitions. The anterior palmar recess was measured from scanning position 6, in the point of maximum distension.
The aspect of the metacarpal head cartilage was verified from the scanning position number 2 with the joint flexed 90° (homogeneity, sharpness of the contour, and the con- stant width were noted). The necessary time for examina- tion was recorded for every subject and every investiga- tor. Al the US images considered representative for every scanning position realized were archived (4 pairs of scan- ning position). At the end of the study the results obtained were analyzed by team A and B and inconsistencies that occurred within each team of examiners were resolved by consensus after reanalysis of archived images.
Statistical analysis
Data were expressed as percentage and means±standard deviation (SD). The 95% confidence interval for mean was calculated. The chi-squared test or Fisher exact test for comparing categorical data was used. P ≤ 0.05 was considered statistically significant.
Independent sample t-test was used to compare quan- titative data. Interobserver agreement (concordance) was calculated using the kappa (Cohen’s kappa) statistics.
Association (linear correlation) between variables was determined by the Pearson correlation coefficient. Data evaluation and statistical analysis were performed with Office Excel SPSS program 19.0 version.
Results
The study subjects were divided into 3 groups accord- ing to age (30-39 years, 40-49 years, and 50-58 years).
The demographic characteristics of the enrolled subjects are detailed in table I.
The results of the US evaluation of the MCF joints are detailed in table II. Erosions were detected more often by the experienced team (p<0.05 referring to the number of joints detected with erosions, p>0.05 refer- ring to the number of patients) and moderate agree- ment (mean kappa agreement 0.567) was obtained.
The agreement inside the team A (with high experience in US) in the detection of the erosions was very good (kappa value 0.83). The erosions were found more of- ten on the radial scan of the second MCP (10 erosions, Fig 1. The scanning positions (longitudinal scans) in a second metacarpophalangeal joint (the metacarpal head – MC – is drawn): 1 – dorsal ulnar (a); 2 – dorsal central (b); 3 – dorsal radial (c); 4 – radial (d); 5 – volar radial (e); 6 – volar central (f) – the palmar recess between calipers; 7 – volar ulnar (g); e) the longitudinal scan of the metacarpal cartilage.
presence of grade 1 signal only in the dorsal scan (scan- ning position 2).
Discussions
The results of our study showed that in healthy subjects, in MCP 2 and 5, chronic lesions (erosions, osteophytes) oc- casionally can be found but signs of inflammation, espe- cially acute inflammation (synovitis), are not present.
The problem of the interpretation of grade 1 synovi- tis (pathological findings or normal aspect) in the finger joints is of real importance. In our study, the experienced team found no joint with the aspect resembling grade 1 synovitis. When reanalyzed, the four cases interpreted as grade 1 synovitis (archived imagined) by team B (be- ginners), we concluded that the hypoechoic areas repre- sent anisotropy, not synovitis. All 4 scans were from the dorsal part of the MCP (scanning position 2). So, in our opinion the aspect of grade 1 synovitis from the palmar scan can be considered pathologic when an examination is performed using an 18 MHz transducer. From the dor- sal scan the interpretations have to be made with caution (especially if no other pathological/clinical findings are present or the experience of the operator is limited), only after the exclusion of the anisotropy artifact.
The dorsal side of the MCP joint is covered by a thicker capsule that forms a dorsal plate [19]. Boutry et al 71.4%), only in subjects over 40 years old, 8 of them
being females. Of note, that one subject had 3 erosions (a 58 years-old female) and in 3 subjects we found 2 erosions (all in the third group of age). A moderate posi- tive correlation was obtained between the presence of erosions and age (r=0.401, p=0.004). Osteophytes were identified in our asymptomatic subjects only on the dorsal scan (scanning position 2), in subjects over 50 years, with a moderate intrerobserver agreement (kappa value 0.421). Concerning the synovitis, team B identi- fied grade 1 synovitis in 2 subjects from the second age- group and in 2 subjects in the third age-group, 3 of them being females. No grade 1 synovitis was observed by team A (p<0.05). All cases with grade 1 synovitis aspect were identified from the dorsal scan (scanning position 2) in the first ten subjects examined by the members of team B (beginners). The dimensions of the palmar recess of both MCP joints had a large distribution (MCP 2 between 0.55-1.3 mm; MCP 5 between 0.6-1.2 mm).
No statistical significant differences were obtained when comparing the dimensions of the two hands or the values obtained in age-groups (all p>0.05). No statisti- cal significant correlations were obtained between the dimensions of palmar recess and height, weight, BMI, or dominant hand (all p>0.05). No pathological findings were found in the examination of the metacarpal head cartilage. PD investigation of the MCP joints found the
Table I. Demographic data of the study subjects.
Characteristics/age group 30-39 years 40-49 years 50-58 years
Number of subjects (%) 24 (48%) 14 (28%) 12 (24%)
Female/male 18/6 10/4 9/3
BMI (kg/m2) 24.43 26.97 29.93
Physical activities moderate moderate moderate
Dominant hand: right/left 22/2 13/1 12/0
BMI-body mass index
Table II. The findings of metacarpophalangeal joint US examination.
Team A Team B P value
N patients N joints N patients N joints N patients N joints
Erosions 9 (18) 14 (7) 4 (8) 4 (2) 0.137 0.016
Osteophytes 4 (8) 7 (3.5) 1 (2) 3 (1.5) 0.168 0.200
Grade 1 synovitis 0 0 4 (8) 7 (3.5) 0.117 0.015
Power Doppler signal 4 (8) 5 (2.5) 3 (6) 3 (1.5) 0.151 0.132
Palmar recess (mm)
Right MCF 2 0.849±0.144 0.905±0.174 0.026
Left MCF 2 0.877±0.145 0.844±0.135 0.161
Right MCF 5 0.849±0.164 0.836±0.191 0.701
Left MCF 5 0.882±0.205 0.816±0.167 0.032
Examination time (min) 7.8±1.74 13.78±2.96 <0.001
Values are expressed as number of patients/joints (%) or mean±SD. N (number) patients= 50; N (number) joints=
200
[14] found in a cadaver study that this structure is a thick yellowish tissue consisting of vascularized connective tis- sue. The US appearance of the dorsal plate in 30 normal volunteer (visible and analyzable in almost all 120 MCP joints) was of a slightly echoic and homogenous structure between the two bones, firmly attached to the base of the proximal phalanx and more loosely inserted at the meta- carpal bone level [14]. This plate is in fact the source of the hypoechoic aspect when the US examination is not perfect perpendicular. Also, Boutry et al [14] specify the possibility that this plate can have the apex pointed (more frequently- 78%) or truncated (we exemplified these as- pects in fig 3). Especially in the last case, the “quantity”
of hypoechoic content of the joint is increased and can be misinterpreted as “filling the angle between the periarticu- lar bones, without bulging over the line linking tops of the bones” as Szkuldarek el al [8] defined grade 1 synovitis.
The dorsal recess is the larger recess of the joint [20,21], with lengths between 6-18 mm [20] and is con- stantly seen on US examination [14]. The articular cavity is quite spacious in the dorsal part of the joints as the capsule in this region is weaker [20,22]. This means that in extension positions the pressure in the dorsal part of the MCP is not high and, if the US examination is correct, without application of the transducer over the skin, the normal vascularisation of the dorsal plate may be seen in some subjects. For this reason the presence of PD signal without an aspect of grey-scale synovitis should be con- sidered normal, not subclinical synovitis.
On the palmar side, the palmar plate, that consists of tight, inflexible, fibrocartilagenous structure tissue [20,22] with different widths and lengths between fingers [23], is blended with a palmar capsule and in the exten-
sion position of the finger, the small vessels are com- pressed [20,22]. This is probably the explanation why we did not find PD signal on the volar side of MCP. Millot et al [10] found PD signal in 5 of 127 healthy subjects included in study. The authors do not mention the sides were the PD was found but they published an US im- age with a PD signal from the dorsal side of the joint.
Probably the same explanation is valuable for the grade 1 synovitis, due to its incipient pathologic vasculariza- tion: in the presence of grade 1synovitis the PD signal was much frequent detected in the dorsal side (28.1%) comparing with palmar side (3.7%) [12]. Also, Witt et al [24] found in patients with newly diagnosed rheumatoid arthritis (RA) more pathologic findings in grey-scale US from the palmar approach and more frequent PD signals from the dorsal approach of the finger joints. In the study realized by Zufferey et al [25] the grade 1 PD signal was found only in 5% of normal volunteers (the authors did not specify the joints where this was found) and they con- sidered to be relevant this grade of PD vascularization for the evaluation of remission in RA patients.
The dimensions of the proximal palmar recess had a large distribution in our study that demonstrates the vari- ous anatomical situations. Taking in consideration the an- atomical previously discussed aspects, we agree with El- legaard et al [9] that in the presence of small quantities of synovial fluid or incipient proliferated synovium, these findings can be demonstrated only in the proximal ante- rior recess, a place where the pressure is low. In this situ- ation, as the finding that synovitis “with extension to at least one of the bone diaphyses” [8] confer at least grade 3 of proliferated synovium, the modifications in the pal- mar proximal recess could be an important factor for the overestimation of the pathological findings and should be taken into consideration. The fact is more important as it was demonstrated that synovitis is more frequently detected on the palmar side compared to the dorsal side [6,12,26,27]. The necessity to define a cutoff of signifi- cant synovitis [25] is important for the delimitation of a normal anterior proximal recess from a pathological one.
The presence of erosions in the healthy popula- tion was already demonstrated in other published stud- ies. Millot et al [10] found bone erosions in 11% joints (MCP 2-5 and fifth metatarsophalangeal joints) of the 127 healthy subjects studied, the MCP 2 being the sec- ond place where the erosions were found (5 cases).
No vascularization was detected within these erosions.
Szkudlarek et al [11] detected in 20 subjects 10 erosions at MCPs (4.2%) level using MRI (3 mm slice thickness) but no erosions were detected by using US. The authors explained the difference between MRI and US by the visualization by MRI of the subchondral cysts that were Fig 3. Dorsal longitudinal scan of the metacarpophalangeal
joint:the dorsal plate with apex a) pointed and b) truncate.
interpreted as erosions. Ejbjerg et al [28] detected low grade erosion-like changes in 2.2% of MCP examined by MRI in 28 normal subjects, especially in the second and the fifth MCP joints. All the lesions were small, without increased signal intensity on postcontrast images.
The presence of osteophytes characterize the hand osteoarthritis [29-31]. We found osteophytes in 7 joints but in the absence of other pathological findings, espe- cially cartilage abnormalities, we could not interpret their presence as belonging to osteoarthritis. Because all the subjects were above 50 years probably these osteophytes were the first imaging findings of a future MCP osteoar- thritis. We found no abnormalities of the metacarpal head cartilage in our subjects and this aspect is important as US is considered to be a reliable imaging modality for the detection of cartilage abnormalities [32].
One important target of our study is the comparison between the 2 teams: the experienced and un-experienced teams. The learning curve in musculoskeletal US was found to be an important aspect in the time of gaining skills in beginner ultrasonographers [33-35]. The 2 be- ginner members of team B rapidly achieved knowledge about MCP examination. The time for an examination was longer compared with the experienced team but with the increasing of the number of subjects examined, this time was improved (for example 20 min the first subject examined and 12 minutes the last one). It has to be un- derlined that the necessity to archive one representative US image from every scanning position increased the examination time in both teams. So, the need for a good training is mandatory in order to obtained reproducible and clinical relevant data from US examinations.
Our study has a number of limitations. First the small number of subjects enrolled does not permit the draw- ing of clear conclusions regarding the frequency of the pathological findings in normal subjects. The lack of sub- jects with intense physical activities in daily life makes it impossible to correlate these findings with mechanical origins of the erosions or osteophytes. Also, we did not compare the US findings with other imaging techniques and with findings in patients with MCP pathology.
In conclusion, in healthy subjects, the pathological findings are occasionally encountered, especially with regard to erosions and osteophytes. Using an 18 MHz transducer the aspect of grade 1 synovitis was not en- countered in healthy non-inflammatory MCP joints. The moderate agreement between experienced and un-experi- enced examiners demonstrated the need for an appropri- ate training for performing musculoskeletal US.
Acknowledge: We want to thank Dr Laura Poanta for the anatomical drawings.
Conflict of interest: none References
1. Naredo E. Ultrasound in Rheumatology: two decades of rapid development and evolving implementation. Med Ul- trason 2015; 17: 3-4.
2. Naredo E, Bonilla G, Gamero F, Uson J, Carmona L, Laffon A. Assessment of inflammatory activity in rheumatoid ar- thritis: a comparative study of clinical evaluation with grey scale and power Doppler ultrasonography. Ann Rheum Dis 2005; 64: 375-381.
3. Kane D, Balint PV, Sturrock RD. Ultrasonography is supe- rior to clinical examination in the detection and localization of knee joint effusion in rheumatoid arthritis. J Rheumatol 2003; 30: 966-971.
4. Luukkainen R, Sanila MT, Luukkainen P. Poor relationship between joint swelling detected on physical examination and effusion diagnosed by ultrasonography in glenohumer- al joints in patients with rheumatoid arthritis. Clin Rheuma- tol 2007; 26: 865-867.
5. Wakefield RJ, Balint PV, Szkudlarek M, et al. Musculoskel- etal ultrasound including definitions for ultrasonographic pathology. J Rheumatol 2005; 32: 2485-2487.
6. Backhaus M, Ohrndorf S, Kellner H, et al. Evaluation of a novel 7-joint ultrasound score in daily rheumatologic prac- tice: a pilot project. Arthritis Rheum 2009; 61: 1194-1201.
7. Scheel AK, Hermann KG, Kahler E, et al. A novel ultra- sonographic scoring system suitable for analyzing finger joint inflammation in rheumatoid arthritis. Arthritis Rheum 2005; 52: 733-743.
8. Szkudlarek M, Court-Payen M, Jacobsen S, Klarlund M, Thomsen HS, Østergaard M. Interobserver agreement in ultrasonography of the finger and toe joints in rheumatoid arthritis. Arthritis Rheum 2003; 48: 955-962.
9. Ellegaard K, Torp-Pedersen S, Holm CC, Danneskiold- Samsøe B, Bliddal H. Ultrasound in finger joints: findings in normal subjects and pitfalls in the diagnosis of synovial disease. Ultraschall Med 2007; 28: 401-408.
10. Millot F, Clavel G, Etchepare F, et al; Investigators of the French Early Arthritis Cohort ESPOIR. Musculoskeletal ultrasonography in healthy subjects and ultrasound criteria for early arthritis (the ESPOIR cohort). J Rheumatol 2011;
38: 613-620.
11. Szkudlarek M, Klarlund M, Narvestad E, et al. Ultrasonog- raphy of the metacarpophalangeal and proximal inter- phalangeal joints in rheumatoid arthritis: a comparison with magnetic resonance imaging, conventional radiography and clinical examination. Arthritis Res Ther 2006; 8: R52.
12. Witt M, Mueller F, Nigg A, et al. Relevance of grade 1 gray- scale ultrasound findings in wrists and small joints to the assessment of subclinical synovitis in rheumatoid arthritis.
Arthritis Rheum 2013; 65: 1694-1701.
13. Bielefeld T, Neumann DA. The unstable metacarpophalan- geal joint in rheumatoid arthritis: anatomy, pathomechan- ics, and physical rehabilitation considerations. J Orthop Sports Phys Ther 2005; 35: 502-520.
14. Boutry N, Lardé A, Demondion X, Cortet B, Cotten H, Cot- ten A. Metacarpophalangeal joints at US in asymptomatic volunteers and cadaveric specimens. Radiology 2004; 232:
716-724.
15. Theumann NH, Pfirrmann CW, Drapé JL, Trudell DJ, Resnick D. MR imaging of the metacarpophalangeal joints of the fingers: part I. Conventional MR imaging and MR arthrographic findings in cadavers. Radiology 2002; 222:
437-445.
16. Theumann NH, Pessis E, Lecompte M, et al. MR imaging of the metacarpophalangeal joints of the fingers: evaluation of 38 patients with chronic joint disability. Skeletal Radiol 2005; 34: 210-216.
17. Tan AL, Tanner SF, Conaghan PG, et al. Role of metacar- pophalangeal joint anatomic factors in the distribution of synovitis and bone erosion in early rheumatoid arthritis.
Arthritis Rheum 2003; 48: 1214-1222.
18. Zayat AS, Freeston JE, Conaghan PG, Hensor EM, Emery P, Wakefield RJ. Does joint position affect US findings in inflammatory arthritis? Rheumatology (Oxford) 2012; 51:
921-925.
19. Takagoshi H, Hashizume H, Nishida K, Masaoka S, Asaha- ra H, Inoue H. Fibrous structure and connection surround- ing the metacarpophalangeal joint. Acta Med Okayama 1998; 52: 19-26.
20. Bade H, Koebke J, Nieden A. Radiologic anatomy of the metacarpophalangeal joints II to V. Surg Radiol Anat 1997;
19: 323-327.
21. McNally EG. Ultrasound of the small joints of the hands and feet: current status. Skeletal Radiol 2008; 37: 99-113.
22. Wise KS. The anatomy of the metacarpo-phalangeal joints, with observations of the aetiology of ulnar drift. J Bone Joint Surg Br 1975; 57: 485-490.
23. Kömürcü M, Kirici Y, Korkmaz C, Alemdaroğlu KB, Sanisoğlu Y, Başbozkurt M. Morphometric analysis of metacarpophalangeal and proximal interphalangeal palmar plates. Clin Anat 2008; 21: 433-438.
24. Witt MN, Mueller F, Weinert P, et al. Ultrasound of syno- vitis in rheumatoid arthritis: advantages of the dorsal over the palmar approach to finger joints. J Rheumatol 2014; 41:
422-428.
25. Zufferey P, Möller B, Brulhart L, et al. Persistence of ultra- soundsynovitis in patients with rheumatoid arthritis fulfill-
ing the DAS28 and/or the new ACR/EULAR RA remission definitions: results of an observational cohort study. Joint Bone Spine 2014; 81: 426-432.
26. Vlad V, Berghea F, Libianu S, et al. Ultrasound in rheuma- toid arthritis: volar versus dorsal synovitis evaluation and scoring. BMC Musculoskelet Disord 2011; 12: 124.
27. Ohrndorf S, Halbauer B, Martus P, et al. Detailed Joint Re- gion Analysis of the 7-Joint Ultrasound Score: Evaluation of an Arthritis Patient Cohort over One Year. Int J Rheuma- tol 2013; 2013: 493848.
28. Ejbjerg B, Narvestad E, Rostrup E, et al. Magnetic reso- nance imaging of wrist and finger joints in healthy subjects occasionally shows changes resembling erosions and syno- vitis as seen in rheumatoid arthritis. Arthritis Rheum 2004;
50: 1097-1106.
29. Hammer HB, Iagnocco A, Mathiessen A, et al. Global ultrasound assessment of structural lesions in osteoarthri- tis: a reliability study by the OMERACT ultrasonography group on scoring cartilage and osteophytes in finger joints.
Ann Rheum Dis 2014 Dec 17. doi: 10.1136/annrheum- dis-2014-206289.
30. Keen HI, Wakefield RJ, Grainger AJ, Hensor EM, Emery P, Conaghan PG. Can ultrasonography improve on radio- graphic assessment in osteoarthritis of the hands? A com- parison between radiographic and ultrasonographic detect- ed pathology. Ann Rheum Dis 2008; 67: 1116-1120.
31. Keen HI, Lavie F, Wakefield RJ, et al. The development of a preliminary ultrasonographic scoring system for features of hand osteoarthritis. Ann Rheum Dis 2008; 67: 651-655.
32. Iagnocco A, Conaghan PG, Aegerter P, et al. The reliability of musculoskeletal ultrasound in the detection of cartilage abnormalities at the metacarpo-phalangeal joints. Osteoar- thritis Cartilage 2012; 20: 1142-1146.
33. Filippucci E, Unlu Z, Farina A, Grassi W. Sonographic training in rheumatology: a self teaching approach. Ann Rheum Dis 2003; 62: 565-567.
34. Gutiérrez M, Di Geso L, Rovisco J, et al. Ultrasound learn- ing curve in gout: a disease-oriented training program. Ar- thritis Care Res (Hoboken) 2013; 65: 1265-1274.
35. Ok JH, Kim YS, Kim JM, Yoo TW. Learning curve of of- fice-based ultrasonography for rotator cuff tendons tears.
Knee Surg Sports Traumatol Arthrosc 2013; 21: 1593- 1597.
