European Journal of Vascular & Endovascular Surgery
Volume 39, Issue 6 , Pages 787-794, June 2010

Advanced Chronic Venous Insufficiency is Associated with Increased Calf Muscle Deoxygenation

Department of Plastic and Reconstructive Surgery, Tokyo Women's Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo 162-8666, Japan

Received 18 September 2009; accepted 31 January 2010. published online 15 March 2010.

Article Outline

Abstract 

Objective

To determine the temporal relationship between changes in calf muscle deoxygenated haemoglobin (HHb) measured by near-infrared spectroscopy (NIRS) during light-intensity exercise and clinical stages of chronic venous insufficiency (CVI).

Design and methods

Calf muscle HHb level was obtained in 168 limbs of 158 patients with various clinical stages of CVI. Clinical manifestations were categorised according to the CEAP classification (CEAP, clinical, etiological, anatomical and pathophysiological), and the patients were divided into two groups: early CVI (C0−3,Ep,s,As,d,p,Pr,o) and advanced CVI (C4−6,Ep,s, As,d,p,Pr,o). Calf venous blood-filling index (FI-HHb) was calculated on standing, then the calf venous ejection index (EI-HHb) was obtained after one tiptoe movement and the venous retention index (RI-HHb) after 10 tiptoe movements.

Results

A total of 116 limbs had early, and 52 had advanced CVI. FI and RI were significantly increased in patients with advanced CVI compared with those with early CVI (P = 0.003, 0.0001, respectively). Similarly, RI was significantly greater in patients who had superficial, combined with deep and/or perforator, insufficiency than in patients with superficial insufficiency alone (P = 0.002). RI showed the strongest correlation with duplex-derived peak reflux velocity in the popliteal vein (r = 0.78, P < 0.0001). Combination of an optimal cut-off point of 0.2 for FI and 2.9 for RI improved the ability to discriminate early from advanced CVI, with a sensitivity of 94% and a specificity of 86%.

Conclusions

These results suggest that FI and RI, as measured by NIRS, may be promising parameters for discriminating early CVI from advanced CVI.

Keywords: Chronic venous disease, Near-infrared spectroscopy, Duplex scanning, Clinical severity

 

Advanced chronic venous insufficiency (CVI) is associated with primary valvular insufficiency (PVI) or post-thrombotic syndrome (PTS).1, 2, 3, 4, 5 Duplex scanning augmented by colour duplex ultrasound imaging has been developed over the last decade and is now a useful tool for identifying venous obstruction as well as venous reflux. An ultrasound-derived reflux time (RT) of ≥0.5 s has been used to indicate the presence of venous reflux.6, 7, 8 However, recent studies have shown that RT does not correlate with the magnitude of reflux, or may not be a useful variable.9, 10, 11

Quantitative direct estimation of O2 supply to the calf muscle during exercise by sampling arterial blood is difficult in humans. Near-infrared spectroscopy (NIRS) is a non-invasive optical method for determining tissue oxygenation and haemodynamics. Using a modification of the Lambert–Beer law,12 today it is possible to obtain quantitative values for levels of tHb, oxygenated haemoglobin (O2Hb) and deoxygenated haemoglobin (HHb). NIRS measurements primarily reflect changes in the small arterioles, capillaries and venules.13 Thus, any change in HHb is presumably a consequence of a change in O2 extraction and microvascular deoxygenation at the site of O2 exchange, and reflects the balance between O2 delivery and O2 utilisation in the localised region of the muscle being investigated by the NIRS system.14 The reproducibility of forearm blood flow determination by NIRS using the venous occlusion method has been shown to be reliable within the test session.15 Recent studies have demonstrated the validity of NIRS for non-invasive measurement of tissue oxygenation in patients with peripheral arterial disease.16, 17, 18, 19 On the other hand, several investigators have attempted to define the severity of CVI by measuring changes in HHb, and concluded that NIRS might be useful for the assessment of ambulatory venous function in PVI and for predicting PTS in the early phase of deep vein thrombosis (DVT).20, 21, 22, 23

In the present study, we evaluated venous reflux using duplex scanning and measured the patterns of calf muscle HHb levels using NIRS. Our primary purpose was to investigate changes in calf muscle HHb during exercise in patients with CVI, and to determine the temporal relationship between changes in calf muscle HHb during light-intensity exercise and the clinical stage of CVI. Furthermore, we investigated the relationship between the findings of duplex scanning and calf muscle NIRS.

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Materials and Methods 

Between January 2008 and June 2008, 168 limbs in 158 consecutive patients with various clinical stages of CVI were evaluated. All the patients had symptoms including aching, pain, tightness, skin irritation, heaviness or muscle cramps to some extent. There were 73 male and 85 female patients, ranging from 33 to 98 years (mean: 61 years) of age. We included 59 limbs in patients with a previous confirmed episode of DVT. We excluded those with peripheral arterial disease (ankle–brachial pressure index of <0.9), those with fixed joints, muscle atrophy or weakness, marked obesity and those with limb swelling due to systemic diseases or lymphoedema. We also excluded patients who had previously undergone varicose vein surgery or compression sclerotherapy. This study was approved by the institutional review board and informed consent was obtained from all participants. Patients were examined clinically by a surgeon experienced in the management of venous disease and classified according to the CEAP classification (CEAP, clinical, etiological, anatomical and pathophysiological) of reporting standards in venous disease.24 They were divided into two groups: early CVI (C0−3S,Ep,s,As,d,p,Pr,o) and advanced CVI (C4−6S,Ep,s,As,d,p,Pr,o).

Patients underwent duplex ultrasound investigation (LOGIQ 7 PRO: GE Yokogawa Medical Systems, Tokyo, Japan) with a 5–10-MHz linear array transducer as described previously.7 Reflux in the superficial venous system was evaluated at the sapheno-femoral junction (SFJ), the sapheno–popliteal junction (SPJ) and in the greater saphenous vein in the thigh (GSV). Reflux in the deep venous system was tested in the common femoral (CFV), femoral (FV), popliteal vein (POPV) and gastrocnemius vein (GV). Reflux in the thigh, calf and ankle perforating vein was also recorded. The main ultrasound-derived parameters assessed were vessel diameter (cm), RT (seconds), peak reflux velocity (PRV; cm s−1), mean reflux velocity (MRV; cm s−1) and total reflux volume (TRV; ml) and were calculated using the equation: TRV (ml) = MRV × area (r2) × RT. The vessel cross-sectional area was estimated from the diameter, assuming a circular vessel shape. Reflux times of ≥0.5 s were considered to indicate incompetence. The diagnosis of venous occlusion was based on both, non-compressibility of the vein on B-mode imaging and lack of spontaneous flow on colour Doppler imaging.

The NIRS technique allows real-time monitoring of tissue oxygenation. The light source of the device (OM-200, Shimadzu Co., Kyoto, Japan) consists of three lasers (wavelengths: 780 nm, 805 nm and 830 nm). According to the variations in optical density (OD) at each wavelength, O2Hb, HHb and tHb are calculated on the basis of the Lambert–Beer law12 allowing changes in the concentration of haemoglobin to be calculated.25 Our instrument had a probe containing the light source and two separate detectors fixed at distances of 2.5 cm and 4 cm from the source. The sensor was taped to the posterior aspect of the calf over the medial head of the gastrocnemius muscle. NIRS detects the light absorbance of haemoglobin chromophores to determine tissue oxygenation. Skin colour is also determined by the presence of chromophores, which might affect NIRS measurement to the probe and was therefore not placed over skin showing pigmentation due to venous disease.26 A review by McCully and Hamaoka27 shows light travels in a shallow arc to a penetration depth of about one-half the separation distance into the tissue. The light emitter–detector distance of the probe used in our study was 40 mm, so the penetration depth was estimated to be 20 mm (Fig. 1). Changes in the haemoglobin concentration were calculated as absolute values (in μmol L−1).28

For assessment of ambulatory venous function, measurements were carried out using the standard exercise protocol as for air plethysmography (APG) (Fig. 2).29 The patients rested supine initially with the leg elevated on a foam block for 5 min. Then they adopted a standing position without putting any weight on the leg being studied, resulting in an increase in HHb concentration as the veins filled. The patients were then asked to keep still until a plateau (HHbV) had been reached. Calf venous blood filling index (FI-HHb; μmol L−1 s) was calculated by dividing 90% of the venous blood volume (HHbV90) by the time taken to fill 90% of the venous volume (HHbFT90). Then the patients were asked to perform one tiptoe movement with weight-bearing on both legs, which produced an ejected volume (HHbEV), and then return to the initial position, the changes in HHb being observed. The calf venous ejection index (EI-HHb) was calculated as HHbEI = HHbEV/HHbV. After a new plateau had been reached, the patients were asked to perform 10 tiptoe movements to achieve venous emptying (HHbE) and a subsequent retention (HHbR). The venous retention index (RI-HHb) was determined as HHbRI = HHbR/HHbE. It took approximately 4–5 min to complete the examination and the 10 tiptoe movements were completed within 10 s.

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  • Figure 2 

    NIRS examination. Calf venous blood filling index (FI-HHb) was calculated by dividing 90% of the venous blood volume (HHbV90) by the time taken to fill 90% of the venous volume (HHbFT90). The patient was then asked to perform one tiptoe movement with weight-bearing on both legs, which produced an ejected volume (HHbEV), and then to return to the initial position, the changes in HHb being observed. The calf venous ejection index (EI-HHb) was calculated as HHbEI = HHbEV/HHbV. After a new plateau had been reached, the patient was asked to perform 10 tiptoe movements, allowing venous expulsion (HHbE) and subsequent retention (HHbR). The venous retention index (RI-HHb) was determined as HHbRI = HHbR/HHbE. a, Rest: b, Standing: c, One tiptoe: d, Ten tiptoes: e, Rest.

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Statistical Analysis 

All data were analysed using SPSS software (Version 16.0; SPSS Inc., Chicago, IL, USA). Comparisons of numerical data between groups of patients were made using Student's t test. Chi-squared contingency table analysis was used to evaluate differences between proportions. Comparisons of HHb means among three different distributions of venous insufficiency were tested using one-way analysis of variance (ANOVA) followed by Fisher's PLSD post hoc test. Correlations between NIRS-derived parameters and ultrasound-derived parameters were assessed by simple linear regression. Continuous data were expressed as mean and standard deviation. Statistical significance was defined as P < 0.05.

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Results 

The baseline characteristics of the study patients are shown in Table 1. There was no significant difference in mean age between the groups. The proportion of male patients with advanced CVI was significantly higher. As expected, the proportion of patients with no venous abnormalities was found to be greater in the early CVI group. Venous obstruction was more common in patients with early CVI than in those with advanced CVI but a higher proportion of venous reflux was found in patients with advanced CVI than in those with early CVI. NIRS-derived FI was significantly increased in patients with advanced CVI in comparison to those with early CVI. Similarly, RI was significantly higher in patients with advanced CVI than in those with early CVI. There was no significant difference in the EI value between patients with advanced and those with early CVI.

Table 1. Baseline characteristics of the study patients.
Early CVI (C0−3S,Ep,s,As,d,p,Pr,o)
n = 110 patients		Advanced CVI (C4−6S,Ep,s,As,d,p,Pr,o)
n = 48 patients		p-value
Mean age (yr)64 S.D. 1262 S.D. 10N.S.a
Gender (% male)37 (34%)36 (75%)<0.0001b
Distribution of venous abnormalitiesn = 116 limbsn = 52 limbs
No venous insufficiency (%)22 (19.0)2 (3.8)0.010b
Venous obstruction (%)19 (16%)2 (4%)0.023b
Complete obstruction (%)1 (0.9)0 (0)N.S.b
Partial obstruction (%)18 (16%)2 (4%)N.S.b
Reflux (%)93 (80%)50 (96%)0.007b
Superficial alone (%)42 (36%)22 (42%)N.S.b
Deep alone (%)21 (18%)8 (15%)N.S.b
P alone (%)11N.S.b
Superficial + deep (%)16 (16%)10 (19%)N.S.b
Superficial + perforator (%)8 (7%)8 (15%)N.S.b
Superficial + deep + perforator (%)4 (3%)1 (2%)N.S.b
Deep + perforator (%)10N.S.b

NIRS-derived parameters
FI (μmol/L s)0.10 S.D. 0.030.22 S.D. 0.080.008a
EI0.44 S.D. 0.060.37 S.D. 0.060.153a
RI1.95 S.D. 0.534.31 S.D. 1.910.004a

FI: filling index (FI-HHb), EI: ejection index (EI-HHb), RI: retention index (RI-HHb).

aStudent's t-test. Values expressed as mean and SD.

bPearson's chi-squared test.

To analyse the relationship between patterns of venous insufficiency and NIRS-derived HHb, the distribution of venous reflux was classified as superficial venous insufficiency alone, superficial combined with deep and/or perforator insufficiency and deep venous insufficiency alone (Table 2). There were no significant differences in the values of FI between the three categories. EI was significantly reduced in patients with deep venous insufficiency alone as compared with superficial venous insufficiency alone. Similarly, RI was significantly greater in patients who had superficial combined with deep and/or perforator insufficiency as compared with superficial insufficiency alone.

Table 2. Relationship of venous insufficiency to NIRS-derived HHb.
NIRS-derived parametersSS + D and/or PD
FI (μmol/L s)0.14 S.D. 0.040.19 S.D. 0.080.20 S.D. 0.07
EI0.46 S.D. 0.07a0.42 S.D. 0.120.29 S.D. 0.07
RI2.20 S.D. 0.59b6.12 S.D. 3.154.33 S.D. 1.67

S: superficial venous insufficiency, D: deep venous insufficiency, P: perforator insufficiency. FI: filling index (FI-HHb), EI: ejection index (EI-HHb), RI: retention index (RI-HHb).

aone-way ANOVA followed by Fisher's PLSD post-hoc test. P = 0.043 compared with D.

bone-way ANOVA followed by Fisher's PLSD post-hoc test. P = 0.002 compared with S + D and/or P.

To assess the ability of NIRS-derived parameters to quantify reflux, their relationship to ultrasound-derived parameters was analysed in groups of limbs with GSV reflux as isolated superficial venous insufficiency or POPV reflux as isolated deep venous reflux (Table 3). No meaningful correlation was found between TRV and any of the NIRS-derived parameters in these groups. Vein diameter and RT had no significant correlation with NIRS-derived parameters in the venous segments examined, with the exception of GSV. Similarly, only MRV in SFJ had a moderate positive correlation with RI. In contrast, PRV had a better positive correlation with RI in the SFJ, GSV and POPV, and with EI in the GV (Fig. 3A–C).

Table 3. Correlation between ultrasound-derived parameters and NIRS-derived parameters.
Vein diameterRTPRVMRVTRV
SFJ
FI0.0310.1930.0820.0760.044
EI0.1070.0140.0310.2170.106
RI0.2390.2040.422∗∗0.342∗0.230

GSV
FI0.0100.1390.2310.1230.074
EI0.0280.0780.0420.0740.074
RI0.483∗∗0.339∗0.431∗∗0.2560.165

POPV
FI0.0120.0280.0920.0370.052
EI0.1330.1760.2840.2450.132
RI0.0090.0240.778∗∗∗0.2010.310

GV
FI0.1260.2080.1770.1930.219
EI0.4510.1490.719∗0.1080.513
RI0.3940.2880.5180.3500.195

Correlations between NIRS-derived parameters and ultrasound-derived parameters were assessed by simple linear regression. SFJ: sapheno-femoral junction, GSV: great saphenous vein, POPV: popliteal vein, GV: gastrocnemius vein. RT: reflux times, PRV: peak reflux velocity, MRV: mean reflux velocity, TRV: total reflux volume. ∗P < 0.05, ∗∗P < 0.01, ∗∗∗P < 0.001. FI: filling index (FI-HHb), EI: ejection index (EI-HHb), RI: retention index (RI-HHb).

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  • Figure 3 

    Correlation between ultrasound-derived parameters and NIRS-derived parameters. A, PRV in POPV had the strongest correlation with NIRS-derived retention index (RI−HHb) (r = 0.78, P < 0.0001). B, PRV in SFJ had a relative good correlation with NIRS-derived retention index (RI−HHb) (r = 0.42, P = 0.002). C, PRV in GV had a relatively good correlation with NIRS-derived ejection index (EI−HHb) (r = 0.72, P = 0.029).

We generated receiver operating characteristic (ROC) curves to determine the discriminating power of the HHb cut-off point. From the ROC curves, several conclusions were immediately apparent (Fig. 4A and B). First, an optimal cut-off point of 0.2 for FI had the highest power to discriminate early from advanced CVI with a sensitivity of 80% and a specificity of 82%. Second, the clinical discrimination performance decreased when a single RI cut-off point of 2.9 was used, as compared with that of FI. Finally, EI did not have any power to discriminate early from advanced CVI. Furthermore, a combination of FI > 0.2 and RI > 2.9 improved the ability to discriminate early from advanced CVI with a sensitivity of 94%, a specificity of 86%, a positive predictive value of 64%, and a negative predictive value of 98%.

  • View full-size image.
  • Figure 4 

    Ability of NIRS-derived HHb to discriminate clinical severity. A, An optimal cut-off point of 0.2 for filling index (FI+HHb) had the highest power to discriminate between early and advanced CVI with a sensitivity of 79.6% and a specificity of 81.9% (area under the ROC curve 0.84, 95% CI 0.78–0.89, P = 0.0001). B, Clinical discrimination performance was decreased using a single cut-off point of 2.9 for retention index (RI−HHb) as compared to that of filling index (FI+HHb) (area under the ROC curve 0.71, 95% CI 0.64–0.78, P = 0.0001).

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Discussion 

This study investigated the relationship between changes in calf muscle HHb during exercise and the clinical stages of CVI. The correlation between the findings of duplex scans and calf muscle NIRS was also investigated. Our main findings in this study were that calf muscle HHb as measured by NIRS was significantly increased in human subjects with advanced CVI, and NIRS-derived EI was significantly reduced in subjects with deep venous insufficiency alone as compared with superficial venous insufficiency alone. Similarly, RI was significantly increased in subjects who had superficial combined with deep and/or perforator insufficiency as compared with superficial insufficiency alone. PRV was found to have a better positive correlation with RI in the SFJ, GSV and POPV, and with EI in the GV, and a combination of FI > 0.2 and RI > 2.9 significantly improved the ability to discriminate early from advanced.

The role of duplex scanning for assessment of CVI is well established. We have previously performed segmental quantitative evaluation in all three venous systems in patients with PVI using duplex scanning and found that the PRV was significantly higher in limbs with advanced CVI than in those with early CVI, for both superficial and deep venous insufficiency, and that RT was not useful for discrimination of clinical severity.9 We have studied venous obstruction and measured quantitative reflux by duplex scanning in a population of patients who completed 6 years of follow-up after DVT, and reported that the presence of reflux as reflected by elevated PRV in the POPV (>25.4 cm s−1) and FV (>24.5 cm s−1) was an independent predictor of advanced PTS.30

The first observations of tissue oxygenation using NIRS were made by Jöbsis.31 This technique has been subsequently refined and applied to the study of cerebral haemodynamics.32, 33, 34, 35, 36, 37 By choosing an accurate distance between source and detector, NIRS can provide direct measurements for any muscle of interest, and over the last two decades, many groups have applied this technique for the evaluation of muscle metabolism.16, 17, 38, 39, 40, 41 A simple and common method of calibrating NIRS signals is to use the range of muscle oxygenation caused by arterial occlusion followed by reactive hyperaemia.42 The arterial occlusion method is based on the assumptions that 5–6 min of ischaemia will result in the complete disappearance of O2Hb and that the reactive hyperaemia after occlusion will almost completely eliminate HHb.43 To measure the absolute value, De Blasi et al. applied arterial occlusion to calculate muscle oxygen consumption.44 The application of venous occlusion also allows the calculation of absolute values from NIRS data. Homma et al. also used the venous occlusion method to measure the blood flow index and oxygen consumption index in forearm muscle during graded exercise.45

Interestingly, this study demonstrated a poor correlation between NIRS-derived parameters and duplex-derived RT. RI in this context may better reflect the severity of venous reflux and is vastly superior to duplex-derived RT. This is further supported by the observation that RI was significantly correlated with duplex-derived PRV, which is now regarded as a useful parameter for discrimination of clinical severity. We also demonstrated a poor correlation between NIRS-derived parameters and duplex-derived TRV in patients with superficial and deep venous insufficiency. TRV appears to be a less valuable parameter than PRV for assessment of reflux magnitude.11

Our study had some potential limitations. We only included patients who had completed more than 2 years of follow-up after the initial episode of DVT as having secondary CVI because the diagnosis of PTS relies on clinical signs and symptoms and there is no confirmatory laboratory imaging or functional test. Calf muscle function could have been evaluated using APG, but APG-derived parameters are not reliable when venous obstruction is present. Although a validation study is required, we believe NIRS should work regardless of venous obstruction. NIRS alone does not discriminate between superficial and deep venous disease. To discriminate the two diseases, both duplex scanning and NIRS seem to be necessary for complete evaluation of limbs with CVI. A combination of FI > 0.2 and RI > 2.9 can discriminate early from advanced CVI with high sensitivity and negative predictive value. However, the positive predictive value was 63.5%. This suggests that there are overlapping values between early and advanced CVI.

In this study protocol, one tiptoe movement produced almost the same result as 10 (HHbEV = HHbV) in some patients, whereas others had a significantly lower or higher value of HHbE in comparison with HHbEV. Therefore, the data obtained using one tiptoe movement and 10 tiptoe movements are quite different. However, further investigation will be necessary to clarify which clinical stages yield similar values of HHbEV as HHbE. Furthermore, the normal values of FI, EI and RI, and the differences in these values between male and female patients, should be clarified in the future.

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Conclusions 

FI and RI measured by NIRS are significantly increased in patients with advanced clinical manifestations of CVI. An optimal cut-off point of 0.2 for FI had the highest power to discriminate early from advanced CVI with a sensitivity of 80% and a specificity of 82%. Furthermore, combination of optimal cut-off points for FI and RI provides strong capability for discrimination of early from advanced CVI with a sensitivity of 94%, a specificity of 86%, a positive predictive value of 64% and a negative predictive value of 98%.

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Conflict of Interest 

No significant conflicts of interest are declared.

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Funding 

None.

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Authors' Contributions 

Yamaki T: study conception and design. Nozaki M: critical revision. Sakurai H: acquisition of data. Soejima K: acquisition of data. Kono T: acquisition of data. Hamahata A: acquisition of data.

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PII: S1078-5884(10)00109-7

doi:10.1016/j.ejvs.2010.01.031

European Journal of Vascular & Endovascular Surgery
Volume 39, Issue 6 , Pages 787-794, June 2010

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