Transcutaneous oxygen measurement in stroke: Circulatory disorder of the affected leg?

998

Transcutaneous Oxygen Measurement in Stroke: Circulatory Disorder of the Affected Leg? Frederik C. Lem, MD, Jack de Vries, MD, DSc ABSTRACT. Lem FC, de Vries J. Transcutaneous oxygen measurement in stroke: circulatory disorder of the affected leg? Arch Phys Med Rehabil 1997;78:998-1002. Objective: To identify variances in the microcirculation of the affected leg of stroke patients and to correlate them with a number of variables that are clinically associatedwith a possible circulatory disorder (“cold leg”). Design: Survey. Setting: Large regional (tertiary care) rehabilitation center. Patients: From 93 acute, first-ever stroke patients admitted for stroke rehabilitation, 10 individuals were selected. Patients with vascular or cardiopulmonary pathology and severe cognitive or speech impairments were excluded. Main Outcome Measures: A clinical assessmentof the following variables was performed: subjective complaints of the affected leg, medication, walking performance, degree of lowerleg edema, trophic pathology, voluntary muscle activity of the dorsal flexors of the affected foot, and the degree of spasticity of the calf muscles. The microcirculation of the affected leg was registered via transcutaneous oxygen measurement (TcPo,). Results: The clinical picture associated with a circulatory disorder (“cold leg”) was partially and modestly present in seven patients. The TcPoz values showed no differences between the paretic and nonparetic lower legs, nor did values change in the course of time after stroke: mean 77.9mmHg (range 42-124) versus 86.1 (41-124) after 8 weeks (n = 10, p = .17); 76.9 (45-96) versus 73.1 (50-96) after 14 weeks (n = 9,~ = .38); and 65.8 (44-88) versus 65.8 (37-78) after 20 weeks (n = 8, p = .48). The clinical symptoms could not be objectified in relation to the microcirculation. Conclusions: In selected stroke patients, no differences were established between microcirculation in both lower legs. TcPo, measurement does not seem to be a suitable method for clinical research on this topic. 0 1997 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation

I

N PATIENTS WITH HEMIPLEGIA after stroke, a “cold limb” or “circulatory disorder of the affected leg” is a common clinical observation. This phenomenon has been described by patients, their relatives, and medical staff. The clinical picture is characterized by one or more of the following complaints and symptoms: a limb with a skin discoloration (blue/purple or red), a cold sensation, edema, and dystrophy.

From the Department of Rehabilitation, Sint Maartenskliniek, Nijmegen (Dr. Lem), and Rehabilitation Centre Het Roessingh, Enschede (Dr. de VI&), The Netherlands. Submitted for publication September 18, 1996. Accepted in revised form February 28, 1997. No commercial party having a direct or indirect interest in the subject matter of this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to J. de Vries, MD, DSc, Rehabilitation Centre Het Roessingh, P.O. Box 310, 7522 AH Enschede, The Netherlands. 0 1997 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation ooO3-9993/97/7809-4188$3.00/O

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When and how frequently these symptoms and complaints occur after stroke is not clear from the literature. Several hypotbeses have been suggested to explain the symptoms and complaints as a circulatory problem: paresis may lead to dysfunctioning of the muscle-pump and from this to disturbances in macrocirculation and microcirculation, including edema; spasticity may hinder blood circulation; or an alteration in activity of the sympathetic nerves may give rise to vegetative dysregulation with trophic and circulatory changes in the skin.“4 Because of changes in temperature and color and the often-present edema, circulatory disturbance is seen as the underlying cause. The literature presents a number of conflicting views on skin temperature of the affected side of stroke patients. Ek and coworkers’ found no significant differences in the surface temperatures of both legs of a hemiplegic patient at rest. Others, using thermography, did find significant differences, which were explained on a circulatory basis.6*7Healthy subjects, however, show different skin temperatures in the legs as well, up to 0.5” to 1.o”C.8‘i0 According to several reports, the incidence of dystrophic reactions in the affected limbs of patients with cerebrovascular accidents seems small.1“‘4 Moskowitz and associates15found dystrophic symptoms in about 5%. With respect to the role of the autonomic nervous system, attention has been focused on a symptomatic approach of vasovegetative symptoms,‘6 rather than on explaining the possible dysfunctioning. Thus, only little is known about possible circulatory dysfunctions in the affected limbs of a patient with hemiplegia. If these dysfunctions do exist, we would expect (considering the clinical symptoms mentioned earlier) microcirculation to causethis clinical picture and macrocirculation, if abnormal, to lead to a picture like the one seen in peripheral vascular (arterial) disease. Objectively, microcirculation can be examined by transcutaneous oxygen (TcP02) measurement, intravital microscopy, and laser Doppler flowmeters. TcPO* measurement is, according to the literature,” reliable, simple to carry out, and patient friendly. The purpose of this study was to try to ascertain, in an objective and reliable manner, the surface microcirculation of hemiplegic patients using TcPO, measurement, and, if that were indeed possible, to compare the skin perfusion of the affected side with the unaffected side. The choice was made to study the legs because most of the clinical observations described occur in this area. We aimed at tracing eventual variances in the microcirculation of the affected leg and correlating them with clinical variables that are associated with a circulatory disorder. METHOD Subjects Participants were selected from 93 stroke patients who were referred for inpatient treatment to a rehabilitation center during 12 months. These patients were admitted from surrounding hospitals an average of 6 to 7 weeks after the stroke. To enable actual investigation of the possible effect(s) of stroke on the microcirculation of the affected leg in a hemiplegic patient, it was necessary to exclude those patients who were

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OXYGEN

Table

Age/Sex

Plegic Side

1 2 3 4 5 6 7

70/M 63/F 38/F 45/F 71/M 67/F 51/M

R R L L L L R

98 10

70/F 68/M 46/F

LR L

Subject

Subjective

MEASUREMENT

1: Subject

IN STROKE,

Lem

999

Description

Complaints

Pain

Stiffness

Warm

Cold

Sweat

CObX

Medication

Walking

Edema

Temperature

Dorsiflexors

Spasticity

+ -

+ + + -

+ -

+ + + + -

+ -

+ + -

Y Y N N N Y N

0 0 5 5 4 5 4

1 2 1 2 2 0 0

0 0 2 -1 -1 -1 -1

0 0 0 0 0 0 0

2 1 1 1 1 0 3

-

-

-

N Y

45 5

0 0

-1 0

4

-

: 1

-

.-

+

known to have an abnormality of microcirculation or macrocirculation, disorders in blood gas values, or a previous stroke. The following exclusion criteria resulted: l Intermittent claudication or other symptoms of peripheral vascular disease. l Diabetes mellitus with a distinct polyneuropathy. l Posttraumatic dystrophy. l Venous insufficiency’x or the status after deep venous thrombosis (changes in the trophic state of the skin and soft tissue of a limb).‘u l Heart or lung disorders affecting blood gas values. l Anemia (affecting oxygen transport capacity). l Previous cerebrovascular accident. l Cognitive or speech impairments that would prevent adequate participation in the study. l Abnormal measured segmental blood pressure (SBP) (ie, ankle/arm ratio of <. 85) The following inclusion criterion was employed: an infarction in the flow area of the medial cerebral artery (as shown by computed tomography [CT] or magnetic resonance imaging [MRI]) with the clinical picture of a hemiplegia, enabling the unaffected leg to be used as comparison. Only I2 patients could thus be selected; a pilot study was carried out on 2. Ultimately, 10 patients entered the actual study. These were 4 men and 6 women between the ages of 38 and 77 years (average, 59). Four had right-sided hemiplegia and 6 left-sided. Clinical Assessment The following clinical variables were ascertained by means of interview and physical examinations, with the help of a questionnaire and examination protocol. Sub.jective complaints of the affected leg, ie, pain, stiffness, abnormally warm or cold sensation, abnormal sweat production, abnormal skin color (either pale, blue and/or purple/red), all scored as present (+) or absent (-). Medication (because of effects on macrocirculation and microcirculation). Any medication with a potential effect was noted. For layout reasons in table 1, only the use (Y) or nonuse (N) of any such medication is represented. Walking performance (influence of pump function of the calf muscles). Using a practical classification with a rating scale of 0 to 5, 0 = nonambulatory; I = walking with the aid of a four-wheeled shopper/four-legged rack/behind a wheelchair, 2 = walking with four-legged walking stick, 3 = walking with crutch, 4 = walking with cane, and 5 = unaided gait. Degree of edema in the lower leg (5 grades of severity; 0 = edema absent, 1 = minimal edema, 2 = moderate, 3 = marked, 4 = severe edema*O). Trophic pathology (skin aspect, hair growth, nail growth, and SUIfdCe temperature as opposed to the other lower leg.)

Abnormal skin aspect, hair, and nail growth noted as present (+) or absent (-). Temperature was compared in 3 graduations: 0 = equal to the unaffected side; - 1 = slightly lower; -2 = significantly lower. l Voluntary muscle activity of the dorsiflexors of the foot, based on the Medical Research Council (MRC) muscular strength scale (0 to 5, in which 0 = paralysis, 1 = muscle contraction visible or palpable, 2 = active movement, without antigravity strength, 3 = active movement against gravity, 4 = active movement against externally applied resistance, and 5 = normal muscle strength2’). l Degree of spasticity of the calf muscles (according to the Ashworth scale; 0 = normal tone; I = slight increase in tone; 2 = more marked increase in tone, but limb easily flexed; 3 = considerable increase, passive movement difficult; 4 = limb rigid in flexion or extension**). The patient characteristics are summarized in table 1. Circulatory Assessment Microcirculation was measured with a transcutaneous oxygen monitor with modified Clark-electrode,’ programmed to warm to a temperature of 44°C. To diagnose macrocirculation pathology (not discovered by means of interviews), SBP measures were taken on arm and ankle, and ankle/arm ratios were calculated. Procedure Eight, 14, and 20 weeks after the stroke, the questionnaire and examination protocol with clinical variables were gone through and the circulation measurements (transcutaneous oxygen pressure) carried out. These measurements were always applied to the same patient by the same examiner at the same time of the same day of the week to avoid variable effects from such factors as tiredness, physical therapy, and meals. Additionally, the following applied to the circumstances under which the measurements were carried out: Normal atmospheric pressure and oxygen content (normal room air). Room temperature between 18” and 23”. Patient at rest (in supine position) to stabilize the O2 consumption as much as possible (Details in the literature do not state clearly the effects of gravity on the TcP02 mea.~urements.4~‘9~2”~27) Smoking prohibited from 1 hour before the measurements (because of strong reversible effects on the cutaneous and subcutaneous perfusion*“). Sensor/vascular stabilization time of 15 minutes. Statistical Tests Student t tests were carried out with paired samples of average TcPo* values. Correlation coefficients were obtained on

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TRANSCUTANEOUS

Table

2: Mean

Measurement

OXYGEN

and Range

77.9mm 76.9mm 65.8mm

(42-124) (45-173) (44-88)

paired samples of each TcPo* measurement: between the paretic and the unaffected leg at each measuring point; on TcPo* values paired with each of the clinical variables, namely the different subjective complaints of the leg, walking performance, presence of edema, trophic pathology, voluntary muscle activity, and degree of spasticity. RESULTS Comparison

of Microcirculation

of the Lower

Legs

Table 2 shows the range of the transcutaneous oxygen values in the lower legs. The lower limit of the values (35 to 50mm) gives an indication of the adequacy of the applied selection aided by interviews, physical examination, and SBP measurements, namely, exclusion of peripheral arterial vascular disease (values of <30mmHg in the foot do not occur in healthy test subjectsz9). There is a tendency for the values to decrease over time. Significant differences in the mean TcPo’ values per measurement of the foot between the paretic and the nonparetic legs were not identified. In addition, TcPo’ did not change significantly for either the paretic or the nonparetic leg of the test subjects over time, ie, between the 8th and 20th week after the stroke (table 3). In view of these results, it was not expected that a relationship would be found between the TcPo* values and the studied clinical variables, and this was indeed the case. “The

Cold Leg”

Table 1 summarizes the clinical assessmentdata on the patient sample. Only one patient (5) demonstrated clear trophic pathology: declined hair growth, thickened and deformed nails on all toes, a pallid-pinkish skin color (for reasons of layout, these three aspects were not included in table I), and a distinctly lower skin temperature on the paretic sic then on the nonparetic side. Of the 10 patients, 3 had grade 2 edema, 4 had grade 1, and in 3 patients edema was not present. The skin temperature of 6 patients was slightly lower in the affected leg than in the nonaffected leg; in one patient it was much lower, and in the remaining 3 patients it was equal. Only two patients (1 and 10) had distinct complaints about Table 3: Time Trend of TcPO* (in mm Hg) for the Paretic and Nonparetic Legs Measurement 1

Average TcPOZ Paretic side

Nonparetic

Arch

side

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2

3

73.8 I n = 9, p = .83 I n = 8, p = .I8

76.9 II n = 8. p = .49

65.8 I

75.6 I ” = 9, p = .73 I n = 8, p = .I7

73.1

65.9

II

I

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n = 8. p = .26 I

1997

IN STROKE,

of TcPOz of the Feet of Hemiplegic

Paretic Foot

1. 8 weeks poststroke 2. 14 weeks poststroke 3. 20 weeks poststroke

MEASUREMENT

Lem

Patients

Healthy Foot

n

86.1 (41-181) 73.1 (50-96) 65.8 (37-78)

10 9 8

P

.I7 (NS) .38 (NS) .48 (NS)

the paretic leg (the patient with clear trophic anomalies was not one of them). One patient (1) had notable discomfort from cold, stiffness, and pain during part of the day, with grade 2 spasticity and absence of voluntary muscle activity of the dorsal flexors of the foot (and of the other leg muscles). The 0’ values measured on the paretic/nonparetic foot were 95194 and 173/77mm. Another patient (10) had slight complaints: occasional stiffness with grade 1 spasticity and good voluntary muscle activity (strength grade 4). The following TcPo’ values were measured: 124/84, 64/68, and 88/66mm. Over time (from the 8th to the 20th week), the pattern of complaints did not change; neither did spasticity nor motor functions. Patient 1 progressed from being a nonwalker to a walker with a four-wheeled shopper. Patient 10 could walk independently from the time of the first measurement. DISCUSSION Determination Transcutaneous

of Microcirculation O2 Monitor

Assisted

by the

Performing measurements under stable conditions proved very difficult. The problem was not so much keeping the relevant external (test environment) variables constant; the patient variables formed the problem and this required much time and patience. Even with the slightest (physical) activity, such as quietly talking, a TcPo’ increase of 5 to 6mmHg was registered. This also points to the extent of the sensitivity of the measuring apparatus. Because of a breakdown, the apparatus was out of use for a long time; hence, in the second series of tests only 9, and in the third series only 8 (of the original 10) patient results were available for processing. Sensitive but vulnerable equipment is involved, in which the quality of the results is dependent on both environment and patient-related variables. In the literature, these observations are only partially illustrated. This problem hampers the interpretation and comparison of the results obtained. Consequently, it appears that this method is quite useful for study purposes, because of the high degree of sensitivity, and less suitable for routine use. The placing of electrodes is a potential source of measurement inaccuracy. The TcPo’ sensor was placed on the dorsum of the foot, on a level with the intermalleolar line in a position at the base of the second metatarsal. In using a TcPo* monitor in the study of venous vascular disease, this placement is well described by Quigley and Fa.ri~.~’In studies of peripheral arterial vascular disease it is not always well described.29s31 So it is uncertain as to whether this is the optimal location. There are various opinions concerning the moment in which a stable vascular situation and oxygen tension have been reached, varying from 2 to 20 minutes after implementation of the apparatus.24*32In many studies, as in ours, it was decided on 15 minutes. Because it appeared that the 0’ values did not always stabilize within this period, a longer sensor/vascular stabilization time was used when necessary. Comparison

of the Microcirculation

of the Lower

Legs

To better understand how to interpret the measurement results of microcirculation, it is necessary to know a few important aspects about circulation (and its measurement methods).

TRANSCUTANEOUS

OXYGEN

A distinction should be made between microcirculation and microcirculation. Microcirculation can be subdivided into socalled nutritive and thermoregulatory skin perfusion. The relationship between microcirculation (condition of the large peripheral vessels) and skin perfusion (especially the nutritive aspect) is not clear.“-‘s In this regard, the following factors are important: (I) central factors, ie, arterial blood pressure, cardiac output, arterial oxygen pressure (Pao*), and arterial oxygen saturation (Sao*); and (2) local factors, ie, local blood Bow. O* consumption, and diffusion circumstances (edema and epiderma1 thickness). To evaluate “the circulation” of an extremity (globally), the following clinical parameters are used: temperature, color, trophic state, and arterial pulsations. Objective methods for evaluation of microcirculation are SBP measurement, Doppler

ultrasound, plethysmography, and arteriography. Objectively, if

MEASUREMENT

3. 4.

5. 6. 7.

microcirculation is examined by transcutaneous oxygen measurement. the measured value, as partial blood gas pressure in millimeters of mercury, is a measure of the amount of oxygen available for diffusion to the skin surface under conditions of

8.

a maximum local hyperemia (superficial vasodilation), brought

10.

about by a built-in

sensor heater.” CONCLUSION

In this study there was no difference established in transcutaneous PO’ values of the paretic and nonparetic feet at each measurement or over time. Two of the many recorded PO’ values are likely inaccurate. The highest value of the paretic leg, 173mm in measurement 2 (the closest value to this was 124 in measurement I) and of the nonparetic leg, 18lmm in measurement 1 (nearest to this was 124mm. also in measurement I), were very close to the TcPo* of the air in the examination room, which was constantly about I80mm. These measurements, however, were immediately repeated in the same session and proved consistent. We found no explanation for these values. A relationship was not found between PO*values and clinical variables. The pssible explanation could be an actual absence of the above-mentioned difference within the selected group of patients: or, based on the patient selection criteria, potential differences could have been missed. It is possible that within a randomized group, which includes patients with a peripheral arterial or venous circulation disorder, because of coexistent cardiac, vascular, or pulmonary pathology, the studied clinical picture may be found more frequently

or clearly. Besides, there is still a possible role of autonomic dysregulation. Indications for this are the occurrence of neurovegetative symptoms in certain patients, with, however, no recorded 0’ differences, and in some cases the requirement of an extended sensor stabilization period pointing to a strong sympathetically mediated vasoconstriction. In this study, this factor of autonomic dysregulation has been eliminated on the basis of the working mechanism of the apparatus, which eliminates the local superficial autonomous (vasoconstrictive) regulation by creating local hyperemia. Therefore, transcutaneous oxygen measurement is not a suitable method for research on autonomic dysregulation. Further research is necessary in a randomized population, using a suitable method. ie, laser Doppler flowmetry or intravital microscopy.

9.

I I. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27.

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