Sex differences in calf muscle hemoglobin oxygen saturation in patients with intermittent claudication

Article Outline

• Abstract
• Methods
  • Participants
  • Medical history, physical examination, and anthropometry
  • Gardner treadmill test
  • ABI and ischemic window
  • Hemoglobin StO2 of the calf musculature
  • 6-minute walk test
  • Walking Impairment Questionnaire
  • Ambulatory activity monitoring
  • Statistical analyses
• Results
• Discussion
  • Differences in calf muscle StO2 and claudication in women and men
  • Differences in exercise performance in women and men
  • Limitations
• Conclusions
• Author contributions
• References
• Copyright

Purposes

We tested the hypotheses that women have greater impairment in calf muscle hemoglobin oxygen saturation (StO₂) in response to exercise than men, and that the sex-related difference in calf muscle StO₂ would partially explain the shorter claudication distances of women.

Methods

The study comprised 27 men and 24 women with peripheral arterial disease limited by intermittent claudication. Patients were characterized on calf muscle StO₂ before, during, and after a graded treadmill test, as well as on demographic and cardiovascular risk factors, ankle-brachial index (ABI), ischemic window, initial claudication distance (ICD), and absolute claudication distance (ACD).

Results

Women had a 45% lower ACD than men (296 ± 268 m vs 539 ± 288 m; P = .001) during the treadmill test. Calf muscle StO₂ declined more rapidly during exercise in women than in men; the time to reach minimum StO₂ occurred 54% sooner in women (226 ± 241 vs 491 ± 426 seconds; P = .010). The recovery time for calf muscle StO₂ to reach the resting value after treadmill exercise was prolonged in women (383 ± 365 vs 201 ± 206 seconds; P = .036). Predictors of ACD included the time from start of exercise to minimum calf muscle StO₂, the average rate of decline in StO₂ from rest to minimum StO₂ value, the recovery half-time of StO₂, and ABI (R² = 0.70; P < .001). The ACD of women remained lower after adjusting for ABI (mean difference, 209 m; P = .003), but was no longer significantly lower (mean difference, 72 m; P = .132) after further adjustment for the StO₂ variables for the three calf muscles.

Conclusion

In patients limited by intermittent claudication, women have lower ACD and greater impairment in calf muscle StO₂ during and after exercise than men, the exercise-mediated changes in calf muscle StO₂ are predictive of ACD, and women have similar ACD as men after adjusting for calf StO₂ and ABI measures.

Intermittent claudication is a symptom of peripheral arterial disease (PAD) and is associated with elevated rates of mortality¹, ², ³, ⁴ and morbidity.⁵ Intermittent claudication, which is present in 5% of the United States population aged >55 years,⁶ occurs during ambulation when the peripheral circulation is inadequate to meet the metabolic requirement of the active leg musculature. Women are less likely to report classic symptoms of intermittent claudication than men at all age groups⁷, ⁸ and are more likely to have asymptomatic PAD.⁹ The lower prevalence of intermittent claudication in women may be a consequence of lower levels of physical activity than men,¹⁰ reporting atypical leg symptoms that are not characteristic of the classical history of intermittent claudication,⁸, ¹¹ or a combination of both. Once intermittent claudication is diagnosed, women lead functionally dependent lifestyles⁹, ¹² and have a mortality rate that is twofold higher than men.⁷

Women with intermittent claudication have shorter walking distances to the onset of claudication pain and to maximal claudication pain during standardized treadmill exercise than men, even though their ankle-brachial index (ABI) is similar.¹⁰ This finding suggests that women may have greater muscular ischemia during exercise than men.

We have previously used the noninvasive technique of near-infrared spectroscopy (NIRS) to assess hemoglobin oxygen saturation (StO₂) of the calf musculature during exercise.¹³, ¹⁴ This technique measures total hemoglobin content of the tissue underneath the probe, which corresponds to capillary blood volume.¹⁵ The StO₂ measurement of the calf provides real-time information on the balance between oxygen delivery and oxygen extraction during ambulation.¹³, ¹⁶, ¹⁷, ¹⁸, ¹⁹, ²⁰, ²¹, ²² In patients with intermittent claudication, as muscle metabolic demand increases during increasingly more intense exercise, insufficient blood flow and oxygen are delivered to the calf musculature, resulting in a decline in StO₂. Thus, the change in calf muscle StO₂ during exercise provides clinically useful information on local ischemia in patients with intermittent claudication.

The purposes of this study were to compare the calf muscle StO₂ measured during standardized treadmill exercise between men and women with intermittent claudication and to determine whether calf muscle StO₂ explains sex-related differences in claudication distances. Our hypotheses were that women would have greater impairment in calf muscle StO₂ in response to exercise than men, and that the sex-related difference in calf muscle StO₂ would partially explain the shorter claudication distances of women.

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Methods 

Participants 

Patients who were limited by intermittent claudication secondary to vascular insufficiency were recruited and screened for this study, as described elsewhere.¹⁴ A similar number of men and women are seen in the university vascular clinics and laboratories, which enhanced our ability to recruit a similar number of men and women for this investigation. The procedures used in this study were approved by the University of Oklahoma Health Sciences Center Institutional Review Board. Written informed consent was obtained from each participant before investigation.

Medical history, physical examination, and anthropometry 

Demographic information, height, weight, cardiovascular risk factors, comorbid conditions, claudication history, blood samples, pulse oximeter measurement, anthropometric measures,²³ and a list of current medications were obtained from a medical history and physical examination to begin the evaluation.

Gardner treadmill test 

Patients performed a progressive, graded treadmill protocol until maximal claudication pain, as previously described.²⁴ The initial claudication distance (ICD) and the absolute claudication distance (ACD) were both recorded to quantify the severity of claudication. Exercise capacity was measured by oxygen uptake at peak exercise with a Medical Graphics VO2000 metabolic system (Medical Graphics Inc, St. Paul, Minn). The test-retest intraclass reliability coefficient with these procedures is R = 0.89 for ICD,²⁴ R = 0.93 for ACD,²⁴ and R = 0.88 for peak oxygen uptake.²⁵ Patients who were limited by intermittent claudication on this test were included in this study, whereas those who stopped exercise for other reasons were excluded.

ABI and ischemic window 

As previously described, ABI was obtained from the more severely diseased lower extremity by the Doppler ultrasound imaging technique before and at 1, 3, 5, and 7 minutes after the treadmill test.²⁴, ²⁶ The ischemic window was determined from the reduction in ankle systolic blood pressure after treadmill exercise compared with the resting baseline value.²⁷

Hemoglobin StO₂ of the calf musculature 

Calf muscle StO₂ was measured before, during, and after exercise using a continuous-wave, NIRS spectrometer (InSpectra model 325; Hutchinson Technology Inc, Hutchinson, Minn), an optical cable attached to a 25-mm probe, InSpectra 2.0 software, and a dedicated laptop computer, as previously described.¹⁴ The probe was attached to the skin over the medial gastrocnemius muscle of the more severely affected leg using a double-sided adhesive light-excluding patch.¹³ A baseline measure of calf muscle StO₂ was obtained at rest as patients stood on the treadmill for 2 minutes to allow for equilibration. From the start of treadmill exercise, the minimum StO₂ value, the time taken to reach the minimum value, the absolute and percentage drops in calf muscle StO₂ from rest to the minimum exercise value, and the average rate of decline from rest to the minimum exercise value were obtained. The recovery times for StO₂ to reach one-half of the resting StO₂ value (recovery half-time), to reach the full resting StO₂ value (recovery time), and to reach the maximum StO₂ value were calculated by subtracting the time to end of exercise from the time recovery StO₂ values were observed.

6-minute walk test 

Patients performed an over-ground, 6-minute walk test (6-MWT), and pain-free and total distance walked during the test were recorded.²⁸ The test-retest intraclass reliability coefficient is R = 0.75 for distance to onset of claudication pain and R = 0.94 for total 6-MWT distance.²⁸

Walking Impairment Questionnaire 

Self-reported ambulatory ability was evaluated using the Walking Impairment Questionnaire (WIQ), a validated questionnaire for PAD patients that assesses ability to walk at various speeds and distances, and to climb stairs.²⁹

Ambulatory activity monitoring 

Daily ambulatory activity was assessed using a step activity monitor (Step Watch 3, Cyma Inc, Mountlake Terrace, Wash), as previously described.³⁰ Ambulatory activity was measured during 7 consecutive days in which patients were instructed to wear the monitor during waking hours and to remove it before retiring to bed. The step activity monitor was attached to the right ankle above the lateral malleolus using elastic Velcro straps and continuously recorded the number of strides taken on a minute-to-minute basis. The accuracy of the step activity monitor is >99% ± 1% in patients with intermittent claudication.³⁰

Statistical analyses 

Differences in means of measurement variables in men and women were examined using the independent sample t test. Differences between sexes for dichotomous variables were examined with χ² procedures. A stepwise regression procedure with switching (probability to enter = .1 and probability to remove = .15) was used to select predictive models for ACD. Initially, body mass index and ABI, dichotomous current smoking, and disease status variables were used as the set of possible predictors. The single variable ABI selected by the procedure was then used as a covariate in an analysis of covariance (ANCOVA) comparing ACD in men and women. The set of predictors was expanded to include calf muscle StO₂ variables, and a second prediction model was obtained. An ANCOVA using these model variables as covariates was used to compare ACD in men and women. All analyses were performed using the NCSS statistical package (NCSS Inc, Kaysville, Utah). Statistical significance was set at P < .05. Measurements are presented as means ± standard deviations.

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Results 

The clinical characteristics of men and women with intermittent claudication are summarized in Table I. The groups were similar on all variables (P > .05), except that women were shorter (P < .001) and there was a trend for women to have a lower body weight (P = .076). Exercise performance measures of the men and women are summarized in Table II. Women had lower ACD (P = .001), peak oxygen uptake (P < .001), WIQ speed score (P < .001), WIQ stair climbing score (P = .001), 6-MWT pain-free distance (P = .003), and 6-MWT total distance (P < .001). Furthermore, fewer women walked continuously during the 6-MWT than men (P < .001): 64% of women stopped ambulating at some point during the test. Although not significant, there was a trend for women to have lower ICD (P = .094) and a WIQ distance score (P = .079). No group difference was noted for the ischemic window (P = .300).

Table I. Clinical characteristics of men and women with intermittent claudication

Variables	Men (n = 27)	Women (n = 24)	P
Age, years	69(9)	67(11)	.522
Height, cm	174.4(7.4)	160.9(6.6)	<.001
Weight, kg	85.6(19.0)	76.9(14.7)	.076
Body mass index, kg/m2	28.1(6.0)	29.8(6.0)	.338
Ankle-brachial index	0.69(0.19)	0.61(0.19)	.125
Race, % white	59	38	.121
Current smoking, % yes	33	48	.297
Diabetes, % yes	26	46	.138
Hypertension, % yes	89	79	.451
Dyslipidemia, % yes	78	88	.473

Values are means (SD) or percentage of subjects in each category.

Table II. Exercise performance of men and women with intermittent claudication

Variablesa	Men (n = 27)	Women (n = 24)	P
Initial claudication distance, m	236(151)	170(118)	.094
Actual claudication distance, m	483(258)	265(156)	.001
Peak oxygen uptake, mL/kg/min	15.0(4.4)	10.8(2.9)	<.001
Walking economy, mL/kg/min	10.8(1.8)	9.7(1.6)	.024
Ischemic window, mm Hg × min/m
After graded treadmill test	0.41(0.48)	0.56(0.54)	.300
After walking economy test	0.26(0.45)	0.41(0.59)	.291
6-min walk pain-free distance, m	242(126)	140(89)	.003
6-min walk distance, m	394(88)	277(78)	<.001
6-min walk rating of perceived exertion, score	12.7(2.3)	13.3(3.5)	.484
Walked continuously for 6 min, % of subjects	88	36	.001
WIQ scores, %
Distance	51(32)	35(30)	0.079
Speed	46(21)	25(18)	0.000
Stair climbing	57(25)	32(27)	0.001
Daily ambulatory activity, strides/d	3631(2254)	3275(2443)	0.590

WIQ, Walking Impairment Questionnaire.

Measures of calf muscle hemoglobin StO₂ of men and women with intermittent claudication are summarized in Table III. The time to reach minimum StO₂ occurred more than 4 minutes sooner in women than in men (P = .010). The Fig illustrates the similarity of dependency of ACD on the time to minimum StO₂ in men (R = 0.580, R² = 0.336, P = .002), women (R = 0.622, R² = 0.387, P = .001), and in the total group (R = 0.653, R² = 0.427, P < .0001). In addition, the recovery time for calf muscle StO₂ to reach the resting value after treadmill exercise was prolonged by >3 minutes in women (P = .036). The group results for the remaining variables were similar (P > .05).

Table III. Measures of calf muscle hemoglobin oxygen saturation of men and women with intermittent claudication from start of exercise to maximum recovery

Variablesa	Men (n = 27)	Women (n = 24)	P
StO2 at rest, % saturation	59(18)	51(20)	.120
Minimum StO2, % saturation	18(20)	17(21)	.885
Time to minimum StO2, sec	491(426)	226(241)	.010
Absolute drop in StO2, % saturation	41(20)	34(16)	.146
Drop in StO2, %	72(28)	72(29)	.972
Average rate of decline in StO2 from rest to minimum exercise value, % saturation/s	0.40(0.62)	0.49(0.48)	.553
Recovery half-time of StO2, sec	143(247)	183(253)	.575
Recovery time of StO2, sec	201(206)	383(365)	.036
Recovery time to maximal StO2, sec	618(258)	766(324)	.082
Maximum recovery StO2,% saturation	91(8)	73(21)	<.001

StO₂, Oxygen saturation.

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• Fig. 

  Association between time to minimum calf muscle hemoglobin oxygen saturation (StO₂) and absolute claudication distance (ACD) in men (black circles) and women (white circles) with intermittent claudication.

The regression model predicting ACD of men and women with intermittent claudication is compiled in Table IV. A forward stepwise regression procedure was used to enter into the model predicting ACD, the time to minimum calf muscle StO₂, the average rate of decline in StO₂ from rest to minimum exercise value, the recovery half-time of StO₂ after treadmill exercise, and ABI. The R² of the full model was 0.70, indicating that the four predictors combined to explain 70% of the variance in ACD. The differences in unadjusted and adjusted values of ACD of the groups are reported in Table V. Women had a lower unadjusted ACD than men (P = .001), which remained lower after adjusting for ABI (P = .003), indicating that sex differences in ACD is not attributable to differences in ABI. However, after further adjustment of the StO₂ variables for the three calf muscles, ACD was no longer significantly lower in the women (P = .132).

Table IV. Regression model predicting absolute claudication distance of men and women with intermittent claudication

Variables	Regression coefficient	SE	95% CI	Partial R2a	P
Intercept	−157.13	94.42	−347.31to33.04	...	.103
Ankle-brachial index	244.87	125.42	−7.74to497.47	0.078	.057
Time to minimum calf muscle StO2	0.56	0.12	0.31to0.81	0.311	<.001
Average rate of decline in calf muscle StO2 from rest to minimum value	151.29	65.86	18.65to283.94	0.105	.026
Recovery half-time of calf muscle StO2	0.25	0.10	0.05to0.45	0.123	.016

CI, Confidence interval; SE, standard error; StO₂, hemoglobin oxygen saturation.

Table V. Unadjusted and adjusted absolute claudication distance of men and women with intermittent claudication

Variables	Men (n = 27)	Women (n = 24)	P
ACD unadjusted (meters)	483(50)	265(32)	0.001
ACD adjusted for ABI (meters)	468(40)	281(42)	0.003
ACD adjusted for ABI and calf muscle StO2 variablesa (meters)	401(26)	341(27)	0.132

ABI, Ankle/brachial index; ACD, absolute claudication distance; StO₂, hemoglobin oxygen saturation.

Values are means (SEM).

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Discussion 

The three major findings of this investigation are:

Differences in calf muscle StO₂ and claudication in women and men 

A key measure of calf muscle StO₂ during exercise is the observed time to reach the minimum StO₂ value, because this measure is positively associated with ICD and ACD and negatively associated with ischemic window in patients with intermittent claudication.¹⁴ Women in the current study had a shorter time to reach minimum calf muscle StO₂ than men, suggesting a greater impairment in the increase in capillary blood volume during exercise.¹⁵ That ABI was not different between men and women and that calf muscle StO₂ was predictive of ACD after adjusting for ABI indicates that the microcirculation is important in exercise performance independent of the macrocirculation.

The faster decline in calf muscle StO₂ in women during standardized treadmill walking is a novel finding and provides a possible physiologic explanation for their shorter ACD compared with men noted in this study and in a previous report.¹⁰ Indeed, the time to minimum calf muscle StO₂ was a highly significant predictor of ACD as well as the average rate of decline in StO₂ from rest to minimum StO₂ value and the recovery half-time of StO₂ after exercise. The longer recovery time of calf muscle StO₂ in women is a consequence of the greater impairment in calf muscle StO₂ during exercise than in men. Collectively, these findings suggest that calf muscle StO₂ measured during and after exercise explains sex-related differences in ACD, even after adjusting for ABI.

In contrast to the observation that the ACD was shorter in women than in men, the ICD was not significantly different between the two groups. This finding does not support our previous observation that women have a shorter ICD.¹⁰ The discrepancy between the ICD results from this study and our previous study is most likely due to the smaller sample size of the current study. When the mean difference in ICD between women and men is compared, the results from the two studies are remarkably similar. Women reached ICD 66 meters (28%) sooner than men in this study, which is similar to our previous observation that women attained ICD 63 meters (33%) sooner.¹⁰ The greater ischemic response during exercise in women, as measured by their shorter time to minimum calf muscle StO₂, has less impact on sex-related differences for ICD than for ACD. This is probably a reflection of the time to minimum calf muscle StO₂ during exercise having a weaker association with ICD than with ACD.¹⁴

Differences in exercise performance in women and men 

In addition to having a shorter ACD, the peak oxygen uptake was 28% lower in women than in men. This is an expected finding and supports our earlier observation of a lower peak oxygen uptake in women,¹⁰ indicating that they have lower cardiopulmonary fitness than men. The impaired exercise performance of women during maximal treadmill exercise also is evident during the less intense 6-MWT, where the pain-free walk distance was 42% lower in women than in men, and the total distance covered during the test was 30% lower in women. Furthermore, far fewer women walked continuously for the entire 6 minutes, as nearly two-thirds had to stop at least once during the test. These results support findings from another investigation that women with PAD had a significantly lower 6-MWT distance than men with PAD.⁸ Finally, the women in this study perceived their ambulatory function to be more impaired than men, as their scores on the WIQ walking speed and WIQ stair climbing subscales were lower, which agrees with our previous study.¹⁰

Limitations 

This study has limitations that are associated with the measurement of calf muscle StO₂, as previously described.¹⁴ Briefly, myoglobin may partially contribute to the calf muscle StO₂ measurement, capillary and venular blood having different oxygen saturations that may mix in the local tissue, and the subcutaneous fat thickness directly under the probe may interfere with the measure of calf muscle StO₂. However, we believe these limitations have minimal influence on calf muscle StO₂, as discussed earlier.¹⁴

Another limitation is that differences in body composition between men and women may account for some of the differences seen in this study. In a previous study, we found that lean tissue mass of the legs was associated with peak oxygen consumption in patients with intermittent claudication,³¹ but its relationship with ACD or calf muscle StO₂ is not known. However, we believe that group differences in leg lean tissue mass had minimal affect in the present study because no difference in ACD was found between men and women after adjustment for ABI and calf muscle StO₂ measures, suggesting that other factors did not contribute to sex-differences in exercise performance.

An additional limitation is that hormonal replacement therapy may have altered results, but this is unlikely because only two women were on this regimen. Finally, the results of this study are only applicable to PAD patients who are limited by intermittent claudication, and thus may not be generalizable to patients with different symptomatology.

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Conclusions 

In patients limited by intermittent claudication, women have a lower ACD and greater impairment in calf muscle StO₂ during and after exercise than men, the exercise-mediated changes in calf muscle StO₂ are predictive of ACD, and women have similar ACDs as men after adjusting for calf StO₂ and ABI measures. These data support the hypothesis that the greater impairment in calf muscle StO₂ in women is a physiologic mechanism for their shorter ACD.

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Author contributions 

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References 

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