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Published online before print August 30, 2002, 10.1148/radiol.2251011272
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(Radiology 2002;225:225-231.)
© RSNA, 2002

Musculoskeletal Imaging

Synovial Tissue of the Hip at Power Doppler US: Correlation between Vascularity and Power Doppler US Signal1

Markus Walther, MD, PhD, Harry Harms, PhD, Veit Krenn, MD, Stephan Radke, MD, Stephan Kirschner, MD and Frank Gohlke, MD, PhD

1 From the Departments of Orthopedic Surgery (M.W., S.R., S.K., F.G.) and Virology, Institute for Digital Image Analysis (H.H.), University of Wuerzburg, Brettreichstrasse 11, 97074 Wuerzburg, Germany; and Department of Pathology, Charité, Berlin, Germany (V.K.). Received July 25, 2001; revision requested August 27; revision received January 8, 2002; accepted February 26. Address correspondence to F.G. (e-mail: f-gohlke.klh@mail.uni-wuerzburg.de).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To correlate power Doppler ultrasonographic (US) findings of the vascularity of synovial tissue of the hip joint with the results of histopathologic examination of the same tissue to assess the value of power Doppler US in the visualization of synovitis.

MATERIALS AND METHODS: The hip joints of 24 patients with osteoarthritis (n = 15) or rheumatoid arthritis (n = 9) of the hip joint were examined with US before arthroplasty. The vascularity of the synovial membrane was classified qualitatively by using power Doppler US. During surgery, a section of the synovial tissue examined at power Doppler US preoperatively was resected. The vascularity of the tissue specimen was investigated and graded qualitatively by a pathologist who was not aware of the US findings. Visual qualitative grading was controlled by means of analysis of the US images and histopathologic specimens with a digital image evaluation system. Correlations between power Doppler US and histopathologic examination findings were calculated by using Spearman rank correlation and Pearson correlation tests.

RESULTS: The correlation between the qualitative power Doppler US results and the qualitative vascularity grades was 0.92 (P < .01, Spearman {rho}). The correlation between quantitative and qualitative results was 0.93 (P < .01, Spearman {rho}) for US imaging and 0.97 (P < .01, Spearman {rho}) for histopathologic examination.

CONCLUSION: Study results showed power Doppler US to be reliable for qualitative grading of the vascularity of synovial tissue of the hip.

© RSNA, 2002

Index terms: Hip, arthritis, 442.254, 442.71, 442.77 • Hip, US, 442.12981, 442.12984, 442.12989 • Synovitis, 442.252, 442.785 • Ultrasound (US), power Doppler studies, 442.12981, 442.12984, 442.12989


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The hip joint is involved in up to 40% of patients with rheumatoid arthritis (1). The use of ultrasonography (US) of the hip was already established by the late 1970s. Wilson and colleagues (2) in 1984 were one of the first groups to report on imaging of hip effusion in patients with rheumatoid arthritis. Thus, it seemed appropriate to evaluate synovitis of the hip with power Doppler US, especially after very promising results in the knee joint had been obtained (3).

Power Doppler US characteristically enables one to encode the amplitude of the power spectral density of the Doppler signal rather than the mean Doppler frequency shift that is recorded with conventional color Doppler US methods (4). Conventional color Doppler US is well suited for evaluation of high-velocity blood flow in large vessels but less effective for detection of low-velocity flow at the microvascular level (5–7). The value of power Doppler US in the detection of soft-tissue hyperemia was reported by Newman et al (8) in 1994. The effectiveness of power Doppler US in estimating the fraction of moving blood in tissue (9–11) led to a fast increase in the use of this examination in several medical fields (12–22).

There are quite a few studies on the visualization of the synovial membrane with power Doppler US of osteoarthritis and rheumatoid arthritis (23–27). To our knowledge, Walther et al (3) were the first to compare power Doppler US findings with vascularity of the synovial membrane at the histopathologic level in the knee joint. However, the knee is much more accessible for US examination than the hip, which is covered by soft tissue. Compared with US of the knee, US of the hip requires lower transducer frequencies, which may reduce the image quality and effectiveness of power Doppler US. Difficulties with power Doppler US of the hip were reported by Strouse et al (28). These investigators did not always observe increased flow in children with septic arthritis of the hip.

In clinical practice, information on the vascularity of synovial tissue of the hip would be of great value in several decision-making algorithms for treatment of disease (eg, septic arthritis, reactive arthritis, and rheumatoid arthritis), including monitoring of disease activity.

The purpose of our study was to correlate the power Doppler US findings of the vascularity of synovial tissue of the hip joint with the results of histopathologic examination of the same tissue to assess the value of power Doppler US in the visualization of synovitis.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Twenty-four consecutive patients (10 men, 14 women) with a mean age of 68 years (age range, 33–81 years) were included. The patients were scheduled for total hip arthroplasty from October 1 to December 31, 1999. Nine of the patients fulfilled at least four of the seven American Rheumatism Association criteria for rheumatoid arthritis (29), and 15 had osteoarthritis of the hip joint. Osteoarthritis was diagnosed in patients who had negative C-reactive protein test results and typical signs on conventional radiographs of the hip. All patients had severe hip pain and underwent total hip arthroplasty. All patients gave their written informed consent, and the study was approved by the institutional review board of the University of Wuerzburg.

Qualitative Power Doppler US Analysis
At a maximum of 12 hours prior to surgery, the hip joints were examined with a real-time US scanner (Elegra; Siemens, Erlangen, Germany). US was carried out by using a 5-MHz electronic linear transducer. A standardized longitudinal anatomic section plane along the neck of the femur was used to visualize the anterior capsule. This is the plane normally used to look for hip effusion (Fig 1). Power Doppler US settings were standardized with a pulse repetition frequency of 1,100 Hz. Although greater low-flow sensitivity can be achieved at lower pulse repetition frequencies (8,18,30), in this study, the pulse repetition frequency was adjusted to 1,100 Hz to reduce flash artifact (13,31). This setting worked well in all cases, although in some patients a lower pulse repetition frequency would have been possible.



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  		Figure 1. Drawing depicts power Doppler US examination of the synovial membrane of the hip joint at the anterior capsule (longitudinal view). AOC = area of calibration, AOM = area of measurement and synovial tissue specimen.

 
For optimum sensitivity, the power Doppler US gain was set to that suggested by Rubin et al (9) and Adler et al (32). This setting requires manual elevation of the power Doppler US gain level until the color box is almost uniformly filled with the first indication of color and with only the minimum amount of the next highest signal just beginning to appear. This procedure can be performed either with the transducer wiped clean of gel and contacting only air (15) or after applying the gelled transducer to the patient at the depth of the region of interest (18), which in our study was the iliopsoas muscle close to the ventral capsule of the hip joint (Fig 1). This setting resulted in gains of 63–68 dB (17,26,31,33). With this method of adjustment (9), depth dependency and the effects of blood pressure, medication, heart rate, and blood viscosity are expected to have the same influence on the synovial tissue as they have on the reference tissue of the muscle and are therefore of minor importance for the measurement.

Either of two fully trained and experienced physicians (M.W., S.R.) performed US, which took 10–20 minutes in each patient. Neither physician was aware of the serologic test results. Each hip was evaluated and given a grade of 1–4, which corresponded to the thickness of the synovial tissue: 1 meant no synovial tissue hypertrophy and a thickness of less than 2 mm; 2, mild synovial tissue hypertrophy and 2–5-mm thickness; 3, moderate synovial tissue hypertrophy and 6–9-mm thickness; and 4, marked synovial tissue hypertrophy and thickness greater than 9 mm. Synovial tissue was measured in its entire thickness, starting from the base of implantation. The grade given corresponded to the worst area of thickening detected.

The examiners assessed the extent of joint effusion by measuring the maximum anteroposterior diameter between the neck of the femur and the joint capsule and assigned one of the following grades: 1, no effusion; 2, mild effusion with capsular distention of less than or equal to 5 mm; 3, moderate effusion with capsular distention of 6–10 mm; or 4, marked effusion with capsular distention greater than 10 mm.

Both examiners graded the blood flow in the synovial tissue by using power Doppler US. The power Doppler US signal of the synovial membrane was graded on a scale of 1–4, as prescribed by Newman et al (26): 1 indicated normal or minimal tissue perfusion with either no signal or only a local dark red power Doppler US signal; 2, mild hyperemia with dark red–to-red signal; 3, moderate hyperemia with red-to-orange signal; and 4, marked hyperemia with orange-to-yellow signal. Perfusion was always graded in relation to the surrounding tissue of the iliopsoas muscle. Whenever the two examiners’ results did not match, they examined the patient together and reached a consensus regarding the findings. The US images were transferred to an S-VHS video system (Panasonic, Secaucus, NJ).

Qualitative Histopathologic Analysis
While performing total hip arthroplasty with routine synovectomy and spinal anesthesia, the surgeon (F.G.) obtained a specimen of synovial tissue from the ventral capsule, exactly at the site where power Doppler US was performed prior to surgery. A pathologist (V.K.) graded the degree of vascularity in hematoxylin-eosin– and factor VIII–stained tissue sections as follows: 1 indicated normal or minimal vascularity and 10% or less of the tissue comprised vessels; 2, mild vascularity and approximately 20% of the tissue comprised vessels; 3, moderate vascularity and approximately 30% of the tissue comprised vessels; and 4, marked vascularity and approximately 40% or more of the tissue comprised vessels. The pathologist was not aware of the power Doppler US findings or clinical diagnoses of the patients.

Quantitative Histopathologic Analysis
The hematoxylin-eosin– and factor VIII–stained tissue sections were evaluated with a television-microscope system (Zeiss Axioplan; Carl Zeiss, Oberkochen, Germany) by using a procedure reported on by Krenn et al (34). The measurements (10–30 per slide) were taken from different regions of interest with good histopathologic depiction of the synovial tissue and averaged. A microscope (part of Zeiss Axioplan) was used, and the stained sections were scanned with a color television camera (DXC 830b RGB-color; Sony, San Diego, Calif) and digitized by using a color frame grabber (DT 2871; Data Translation, Marlboro, Mass).

The size of the tissue images was 512 x 512 pixels with a dynamic range of eight bits per color channel and a spatial sampling density of 1.3 pixel/µm. The separation algorithms and calculations were performed on a computer workstation (DEC-Alpha-433-W; Compaq, Houston, Tex).

The brown areas of interest in the tissue, representing blood vessels, were separated on the images, according to the colorimetrics of the television system (35), by using the differences between the red, green, and blue color channels. The color brown is represented by a red-yellow (ie, orange) color containing a small portion of blue. The relationship "red is greater than green, which is greater than blue" can therefore be used to distinguish blood vessels from surrounding tissue on the images (36). The average percentage of brown areas in relation to the whole tissue area is a measure of vascularity in the section and was calculated for further analyses.

Quantitative Power Doppler US Analysis
The S-VHS videotapes were digitized as bit map–formatted images (24 bit). Three images that demonstrated the highest power Doppler US signal in each patient were obtained for further analyses. The areas of calibration on the screen of the US scanner were analyzed by means of color measurement (35) on the computer workstation.

Power Doppler US does not enable direct measurement of vascularity. A low power Doppler US signal, represented by dark red color, indicates a small number of moving red blood cells, and more yellow color indicates a high number of moving red blood cells. An increase in the number of detected blood cells leads to a shift from red to yellow color markings. The parts of the tissue with no detectable blood cells are gray or white.

The number of red-yellow pixels (red > green > blue and blue near zero) is a measure of blood flow and was quantified according to the calibration procedure prescribed by Rubin et al (9) and the manufacturer’s power Doppler US distribution function algorithm. The number of red-yellow pixels was graded on a scale from 0 to 4: 0 represented 0–100 pixels; 0.5, 101–500 pixels; 1.0, 501–1,000 pixels; 1.5, 1,001–1,500 pixels; 2.0, 1,501–2,000 pixels; 2.5, 2,001–2,500 pixels; 3.0, 2,501–3,000 pixels; 3.5, 3,001–5,000 pixels; and 4, more than 5,000 pixels.

Statistical Analyses
Our main interest was the relationship between the power Doppler US findings and the vascularity of the tissue at histopathologic analysis. The pathologist’s judgment regarding the vascularity of tissue was qualitative. The relationship between the two variables was analyzed by using the Spearman rank correlation test.

In contrast, with digital data processing, a numeric (ie, quantitative) value was assigned to the power Doppler US signal and to the vascularity of the tissue. The relationship between these numeric values was determined by using the Pearson correlation test.

The correlation between the qualitative power Doppler US and tissue section results and the quantitative power Doppler US and tissue section results was calculated by using the Spearman rank correlation test to evaluate the reliability of the examiner’s visual interpretations of the tissues sections and power Doppler US images.

Differences between patients with osteoarthritis and those with rheumatoid arthritis were analyzed by using the t test (for numeric variables) and the Mann-Whitney test (for qualitative variables).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Patient characteristics, power Doppler US findings of joint effusion and synovial thickness, and histopathologic findings are provided in the Table. Two examples each of histopathologic and power Doppler US findings are shown in Figure 2. The correlation between the qualitative power Doppler US results and the pathologist’s qualitative vascularity estimations was 0.92 (P < .01, Spearman {rho}).


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  		Power Doppler US and Histopathologic Findings

 


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  		Figure 2. Distinctive features of different grades of synovial tissue vascularity in two patients, as seen in frozen sections stained with hematoxylin-eosin (HE) and factor VIII (middle) and on corresponding longitudinal power Doppler US (PDS) images of the hip.

 
The visual (ie, qualitative) estimations of vascularity based on power Doppler US image and tissue section findings were compared with the results of quantitative image processing by using the Spearman rank test. The correlation between visual (ie, qualitative) and quantitative interpretations of power Doppler US findings was 0.93 (P < .01, Spearman {rho}). The correlation between visual and quantitative histopathologic analysis results was 0.97 (P < .01, Spearman {rho}). Both values were evidence of the reliability of the examiner’s visual interpretations of tissue sections and power Doppler US images.

The Pearson correlation between the results of quantitative analysis of the power Doppler US images and the results of quantitative analysis of the factor VIII–stained tissue sections was 0.91 (P < .01) (Fig 3).



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  		Figure 3. Graph shows correlation between findings at quantitative analysis of power Doppler US and findings at quantitative analysis of factor VIII-stained tissue (Pearson correlation = 0.91, P < .01).

 
We observed a correlation between synovial membrane thickness and power Doppler US signal (Spearman {rho} = 0.80, P < .01). The Spearman {rho} correlation between synovial membrane thickness and tissue section vascularity was 0.84 (P < .01). There was no correlation between synovial proliferation and effusion (Spearman {rho} = 0.26, P = .31).

There was a significantly higher power Doppler US signal in the patients with rheumatoid arthritis according to quantitative (P < .01) and qualitative (P < .01) US findings, as compared with the signal in the patients with osteoarthritis. Quantitative (P < .01) and qualitative (P < .01) analyses of the histopathologic sections revealed a higher degree of vascularity in the patients with rheumatoid arthritis than in those with osteoarthritis. Also, hypertrophic synovium was more frequent in the patients with rheumatoid arthritis (P < .01). Effusion was observed in both groups, without any significant differences.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
Synovial proliferation is the fundamental event in inflammatory arthritis (37). The growth of fibroblast-like synoviocytes and the production of metalloproteinase by fibroblast-like synoviocytes contribute to the cartilage and bone destruction that is associated with hypervascularized tissue that contains fibroblastic elements, which are referred to as pannus (38,39). Joints affected by inflammatory tissue, as seen in rheumatoid arthritis, require specific treatment, such as disease-modifying drugs, local injection of corticosteroids, radionucleotide synoviorthosis, or synovectomy. Visualizing inflammatory tissue is therefore an important element in the diagnosis of and monitoring of disease activity in rheumatoid arthritis.

To date, the predominant examination used to visualize synovial tissue and synovial vascularity at the hip has been magnetic resonance (MR) imaging. The ability to differentiate between effusion and synovial proliferation with MR imaging has been greatly improved by the intravenous application of paramagnetic contrast agents (1,40–46). van Dijke et al (47) demonstrated a technique for measuring abnormal capillary permeability in the synovial tissue of the arthritic knees of rats by using dynamic MR imaging with an intravenously administered gadolinium-based blood pool agent. In their study, MR imaging–derived microvascular characteristics correlated well with histopathologic characteristics. O’Byrne et al (48) compared MR imaging and histopathologic findings in a rabbit model for osteoarthritis and immune arthritis. They reported that MR imaging can be used to observe the therapeutic effects of disease-modifying drugs on synovial inflammation and cartilage degradation in rabbit knees. However, for a detailed assessment of disease progression based on serial MR imaging findings, precise timing and standardization of the MR imaging protocol are required (49–51).

The value of power Doppler US in depicting low-velocity blood flow at the microvascular level in different types of tissue has been proven in studies performed by several authors (8,24,26,30,52–54). Fiocco et al (24) compared conventional US depiction of synovial proliferation with arthroscopic visualization in patients both before and after synovectomy. That group, having observed a significant correlation between clinical and US indexes, stated that US can be used as an objective method to monitor the response of inflammatory knee joint diseases to therapy and reported a significant correlation between clinical and US indexes. Silvestri et al (55) used color Doppler US to monitor the activity of rheumatoid arthritis in the knee joint and found a correlation between vascular findings and clinical symptoms.

The value of power Doppler US in the evaluation of the synovial membrane at the knee joint was demonstrated in a study by Walther et al (3), who correlated power Doppler US findings with vascularity at the histopathologic level. However, the knee joint is easier to access at US than the hip, and transducers with lower frequencies have to be used in the hips of adults.

In our study, effusion was observed in patients with osteoarthritis and in those with rheumatoid arthritis, without any significant differences between the two groups. The correlation between synovial membrane thickness, power Doppler US signal, and tissue section vascularity was in accordance with clinical experience; however, a thick synovial membrane did not always correlate with high disease activity. There was no correlation between synovial proliferation and effusion. Tissue debris, blood clots, and fibrin are known to mimic some US features of synovial proliferation (24) and can be excluded with power Doppler US.

Power Doppler US depicts the movement of blood cells within a vessel. The fact that this movement does not always indicate increased vascularity or hyperemia of the synovium, however, is still a problem in interpreting power Doppler US images (42). Power Doppler US is influenced by the examiner’s skill and experience, the spatial and temporal resolution quality of the US equipment, and the acoustic conditions involved in image processing. Power Doppler US should be performed in addition to conventional US evaluation of an arthritic joint. Power Doppler US assists in determining whether the region of interest shows increased blood flow (31). This information can be important for monitoring local disease activity and distinguishing between hypervascular and fibrous pannus.

To our knowledge, before the present investigation, all studies to assess synovial tissue addressed the knee joint (26,55–57). When Strouse et al (28) investigated septic arthritis of the hip in children, they did not observe increased flow in all patients with infection. The data from a rabbit model confirmed these results (27). In that study, only 23 of 45 power Doppler US examinations of infected knees that were performed 1–6 days after inoculation were unequivocally positive.

To our knowledge, our study is the first in which power Doppler US findings were correlated with histopathologic findings in the synovial tissue of the hip joint in humans. Compared with synovitis of the knee joint, synovitis of the hip joint in adult patients is difficult to assess at clinical examination.

Patients who have groin pain and a reduced range of hip joint motion present with symptoms that are associated with a long list of differential diagnoses. Our study results indicate that power Doppler US is a powerful tool for the objective assessment of synovial tissue perfusion of the hip. The results of power Doppler US, when the examination is performed accurately, have been shown to be as reliable for hip evaluation as they are for knee joint assessment (3).

In the future, the use of US contrast agents and harmonic imaging may increase the potential applications of power Doppler US, because both of these elements greatly enhance color flow sensitivity. However, the limitations of this examination are the dependence on the examiner’s skill and experience, the lack of accepted standards for adjustment of the gain level, and the fact that the dorsal aspect of the hip joint is not accessible with US.

In conclusion, power Doppler US is a reliable and accurate method of visualizing blood flow in the synovial tissue of the hip joint. The highly significant correlation between power Doppler US findings and histopathologic findings supports the value of this imaging technique. Because US is an easy to handle, safe, inexpensive, and noninvasive procedure that is available in most radiology departments, power Doppler US may continue to be an important part of the diagnosis and monitoring of musculoskeletal disorders. Common indications might be control of disease activity, investigations prior to steroid injection, and follow-up of hip joint infections.


   ACKNOWLEDGMENTS
 
Thanks to Jutta Pfeuffer and T. Peter Faehndrich for preparing the tissue sections, to Robert Morrison for support in translating the manuscript, and to Jana Hinterberger for scanning the tissue sections with the microscope-television system.


   FOOTNOTES
 
Author contributions: Guarantors of integrity of entire study, M.W., H.H., V.K., F.G.; study concepts and design, F.G., M.W.; literature research, M.W., S.K.; clinical studies, M.W., S.R.; experimental studies, H.H., V.K.; data acquisition, F.G., M.W., S.R.; data analysis/interpretation, M.W., H.H., V.K.; statistical analysis, M.W., H.H., S.K.; manuscript preparation, M.W.; manuscript definition of intellectual content and editing, M.W., F.G.; manuscript revision/review and final version approval, M.W., H.H., V.K., S.K., F.G.


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TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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