|Year : 2018 | Volume
| Issue : 2 | Page : 80-86
Exercise oximetry in arterial claudication
Pierre Abraham1, Tianyu Ma2, Huifei Chen3, Lianrui Guo2, Yongquan Gu2, Samir Henni4
1 Vascular Medicine, University Hospital; Department of Physiology, Faculty of Medicine, LUNAM University, Angers, France
2 Vascular Surgery Department, Xuanwu Hospital Capital Medical University, Beijing, China
3 Xiangtan Central Hospital Cardiovascular Center, China South University, Xiangya Medical College, Changsha, Hunan Province, China
4 Vascular Medicine, University Hospital, Angers, France
|Date of Web Publication||26-Sep-2018|
Department of Physiology, University Hospital, Angers, France. Faculty of Medicine, Lunam University, INSERM 1083/CNRS 6015, Angers
Source of Support: None, Conflict of Interest: None
Transcutaneous oxygen pressure measurement (TcPO2) is well known as a useful tool for the evaluation of critical limb ischemia, but it is rarely used during exercise (Ex-TcPO2). We have used exercise oximetry, in Angers, as a noninvasive vascular investigation for about >15 years to detect regional blood flow impairment at the proximal and distal levels simultaneously and on both sides. The use of a chest electrode is required to calculate the Delta from rest of oxygen pressure index (DROP) and account for eventual systemic exercise-induced hypoxemia. The DROP index that we proposed in our first publication in 2003, because of its mathematical formula, is independent of the absolute oxygen pressure starting values which result in improved reliability of Ex-TcPO2 as compared to the regional perfusion index. The present review is of specific interest at a time when the technique is rapidly spreading in France and Abroad.
Keywords: Claudication, diagnosis, exertional limb pain, oxygen, peripheral artery disease, treadmill testing
|How to cite this article:|
Abraham P, Ma T, Chen H, Guo L, Gu Y, Henni S. Exercise oximetry in arterial claudication. Vasc Invest Ther 2018;1:80-6
| Introduction|| |
Transcutaneous oxygen pressure measurement (TcPO2) has been used in human for years.,,,,, The absolute value of TcPO2 is generally accepted as part of the definition of critical ischemia in Fontaine Stages 3 and 4, where cutaneous oxygen supply is altered. Since our first study published in 2003, we have used exercise oximetry not only at rest from critical limb ischemia ,, but also at exercise to confirm the arterial origin of limb pain in patients complaining exercise-induced lower limb pain or discomfort when walking.,, The present review illustrates the issues, difficulties that arise about this underused clinical approach.
| History for the Clinical use of Transcutaneous Oxygen Pressure|| |
TcpO2 is scarcely used during exercise, specifically as a diagnostic test. First attempts for exercise oximetry come back to the nineties.,,, Following these initial publications, few authors have reported the use of TcPO2 during exercise (Ex-TcPO2),,,, with the rapid evidence that although the technique was attractive because it allowed recording throughout exercise and accounted for systemic chest PO2 changes, the low reliability of results in test-retest recording was unsatisfactory. Thereby, the technique was almost abandoned in the 1990s until we published our paper in 2003. What was really new about the technique in this paper? As is further developed below, the major point in the 2003 paper is the analysis of results through the Delta from rest of oxygen pressure (DROP) index that gets rid of absolute starting values, and that results in a highly reliable test–retest approach., In the last 3 years, the technique is rapidly spreading in France and abroad., Clearly, there is no interest in using TcPO2 at rest in Fontaine Stage 2; however, it has been proven to be valid in the evaluation of lower limb claudication during exercise.,,,
| Technologies for Recording Transcutaneous Oxygen Pressure|| |
Most available systems use a “Clark type” electrode. In a Clark-type electrode, the system includes a platinum cathode and a silver anode immersed in an electrolyte solution. The electrodes are protected by an oxygen permeable membrane. As the platinum cathode is polarized, oxygen becomes reduced at the cathode surface and acts as an electron acceptor. The current indicates oxygen concentration and pressure.
Recently, a German manufacturer launched a probe based on a photo-reactive concept where the light from a green light-emitting diode excites the sensor spots of a matrix layer to emit fluorescence. If the sensor spot encounters an oxygen molecule, the excess energy is transferred in a nonradiative way, quenching the fluorescence signal. The degree of quenching correlates to the partial pressure of oxygen in the matrix, which is in dynamic equilibrium with oxygen in the sample.
Both systems are measuring oxygen concentration (partial pressure) and should not be confused with the near-infrared spectrometry approach that measures hemoglobin saturation and not tissues partial pressure for oxygen through the absorption of infrared light by hemoglobin.
Transcutaneous measurement of oxygen pressure correlates fairly well with systemic PO2 in neonates., Unfortunately, in adults, the skin thickness results from a transcutaneous gradient and the surface oxygen pressure is lower than the pressure of oxygen in underlying tissues. One important point here is to keep in mind that the unpredictable gradient which results in surface PO2 being lower that tissue PO2 in the adult, is assumed to be constant over time within an experiment.
| Importance of the use of a Chest Electrode in Exercise-Transcutaneous Oxygen Pressure Measurement|| |
During exercise TcPO2 recordings, a chest electrode is generally used, to take into account eventual systemic PO2 changes. This is of particular interest to confirm that local inadequate oxygen supply to fulfill oxygen demand is due to an abnormal blood flow supply and normal systemic oxygen content or to a normal blood flow supply but low oxygen content of the blood due to systemic hypoxemia. The arterial PO2(and then TcPO2) in normal or diseased patients may either increase (due to improved ventilation/perfusion ratio during moderate exercise) or decrease (due to the obstructive or diffusive lesions in the lungs). In the aging population studied, chronic airway diseases are far from being rare. Previous studies have proven that although the transcutaneous to arterial PO2 difference may change from one experiment to another, this difference remains constant during moderate exercise within an experiment thus allowing for continuous monitoring of PaO2 absolute changes over time (although not providing absolute instantaneous values)., The concordance of TcPO2 changes (regardless of starting value) with absolute arterial changes (regardless of starting absolute value) to monitor systemic PO2 changes has been largely validated. Typical examples of simultaneous chest recordings are shown in [Figure 1]. As shown the absolute value may differ, but changes over time are identical. Analyzing chest changes have resulted in the classification of likely normal Types A and B, and of Type C or Type D chest-TcPO2 profiles that are likely to result from abnormal responses.
|Figure 1: Simultaneous recordings of the right and left chest changes in transcutaneous oxygen pressure at rest (first 2 min of recording) during exercise (variable duration shown as a gray rectangle) and recovery (10 min for all recordings). One probe is positioned on each side. Note that, absolute starting values are different but changes over time are similar|
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| The Delta from Rest of Oxygen Pressure Index to Get Rid of the Unknown Transcutaneous Gradient|| |
The meaning of DROP is Delta from Rest of Oxygen Pressure. There are two ways to account for chest PO2 changes. Originally, the one used in the past was to calculate the ratio of limb to the chest, generally referred to as the regional perfusion index (RPI). This RPI has no unit (it is a percent value) and is dependent on the transcutaneous gradient as we previously showed. We do not use it. We use the change from rest (Delta from Rest) of oxygen pressure, which is expressed in mmHg and is inherently independent of the initial transcutaneous gradient as described in our original publication. To calculate DROP, we first calculate the instantaneous value minus resting value at both the limb and chest level. This generally results in a negative value at the limb since in most cases PO2 remains stable or decreases at exercise at the limb level. This often results in a positive value at the chest except in some cases of exercise-induced systemic hypoxemia. Then, we subtract chest changes to limb changes. Thus, if the chest is converted to absolute values, chest changes are added to the negative limb changes when chest TcPO2 increase or subtracted, if chest TcPO2 decreases. As a result, if chest and limb changes are the same due to exercise-induced systemic hypoxemia, the DROP will remain unchanged, though absolute values may decrease. This is clearly of interest to differentiate limb decrease resulting from regional abnormal blood flow supply from those resulting from systemic PO2 changes. The following [Figure 2] illustrates schematic results for DROP calculation.
|Figure 2: Schematic representation of the effect of changes in chest and limb absolute value over delta from rest of oxygen pressure calculation|
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For example, during exercise TcPO2a stable thoracic value can be associated with a 20 mmHg decrease of buttocks values or inversely of stable buttocks value with a 20 mmHg systemic PaO2 increase. In the first case, DROP would be minus 20 mmHg, whereas it would be zero in the second case since buttocks changes directly reflect systemic changes. Inversely stable absolute buttocks values can result in a negative DROP value if thoracic (and then systemic) PO2 increases. For another example, the absence of increase of buttocks values while thoracic TcPO2 increases by 20 mmHg, likely are due to peripheral insufficient perfusion and would result in a DROP value at that buttock of minus 20 mmHg, as well.
| Validation and Indications for Exercise-Transcutaneous Oxygen Pressure Measurement in Patients with Claudication|| |
In evaluating arterial disease, X-ray (arteriography or computed tomography scan) is the “goldstandard.” This is the reason why we studied the ability (sensitivity and specificity.,) of TcPO2 to detect arteriographically proven lesions in patients suspected of proximal claudication, and not on the contrary to study the relationship between TcPO2 and proximal pain in patients with/without the hypogastric arterial disease. Consistently, we have shown that ultrasound which is generally used as a routine investigation in peripheral artery disease (PAD) fails to detect many arterial lesions in patients with proximal claudication. There is no reason that all severe lesions should result is regional ischemia due to the presence of collateral (vicariate) vessels. Then, one should not expect a 100% sensitivity of Ex-TcPO2 compared with imaging. Roughly, Ex-TcPO2 is to be considered a test of the responsibility of PAD in exercise-related symptoms.
The presence of radiographically significant arterial lesions is not necessarily proof that they are responsible for the clinical symptoms. Indeed, due to the frequent association of osteoarticular lumbar or hip lesions and proximal vascular diseases (as clearly illustrated by the studies of L Kauppila),,,,, there is numerous situation where proximal exercise-induced pain may be partly of nonvascular origin in vascular patients. Similarly, ischemia at one specific site can perfectly remain asymptomatic in more severe ischemia at another site (say the calf) results in pain at the other site masking pain at the buttock level. Then, in the validation approach of Ex-TcPO2, the reference cannot be the presence of pain.
| Other Techniques for Exercise Diagnosis in Patients with Peripheral Artery Disease|| |
Ankle to brachial index
Ankle to brachial index (ABI) is cheaper, technically easy, and accessible. Approximately 13.6% of PAD patients have arterial stiffness. Before it results in noncompressible arteries, stiffness may lead to an overestimation of ABI. There is strictly no reason why stiffness shall interfere with results at rest and would not interfere with postexercise results. Then, using an exercise test independent from arterial stiffness is of major interest. Finally, 30% of the patients with arterial claudication and a normal ABI have a decrease below 0.9 after exercise. Although the normal limits to be used in exercise TcPO2 have been clearly defined at the calf and buttock,, there is no consensus as to the normal limit to be used for postexercise ABI as clearly reported recently by Mahé et al.
One very interesting and original point about doing Ex-TcPO2 and not postexercise ABI is the observation of normal TcPO2 results in patients with abnormal resting ABI. To the best of our knowledge, no normal postexercise ABI has even been reported in patients with abnormal resting ABI. We recently reported  the frequency of these observations and underlying conditions for this, among which: proximal claudication and exercise-induced systemic hypoxemia. Proximal ischemia is also one of the major cause of exercise-induced pain in patients with a normal ankle to brachial index at rest  and abnormal chest changes at exercise suggesting impaired systemic oxygenation during exercise which is found in approximately 15% of the patients referred for claudication in our experience. This does not necessarily mean that the patients do not have PAD but rather that many suffer walking limitation from the nonPAD origin.
Thermography has been proposed to objectively measure muscle activity during exercise. It could be proposed to analyze the expected cooling of the diseased leg as compared to the normally perfused leg during exercise., There are few reports confirming the possibility of measuring this phenomenon as well as the “warm knee paradox in popliteal occlusions,”, using thermographic infrared cameras. In our opinion, the accuracy of the system and sensitivity to environmental conditions make this approach of low interest.
Near infrared spectroscopy
Although it is intended to measure muscle values, which are a great advantage as compared to surface TcPO2, near-infrared spectroscopy (NIRS) measures saturation and the sigmoidal relationship of saturation to pressure for oxygen is an important pitfall for the technique. The research with NIRS during exercise in arterial disease remains limited and limited data are available using bilateral measurements during exercise.,,, The use of NIRS on the buttocks might not be a favorable site for NIRS measurement due to subcutaneous fat thickness. This might explain a lower performance as compared to Ex-TcPO2, at least at the buttock level.
Penile pressure measurement
The penile brachial index may be useful for an obviously limited population. At present, it can be routinely used in male patients for the impotence of suspected vascular origin., Since penile pressure measurements are frequently performed, as in our laboratory, with plethysmography rather than Doppler, it would not differentiate between the right and left side. The Doppler is expected to be more side specific, but frequent anatomical variations and anastomoses can be seen which makes the sensitivity and specificity debatable in the case of unilateral lesions. Finally, the results could hardly be obtained during walking. Last, we showed that penile pressure is not relevant to the hypogastric circulation.
Magnetic resonance imaging
Beyond the interest of the technique for injected visualization of vessels before surgery, the recent development of magnetic resonance imaging has led to some interesting physiological research in the field of limb blood flow and limb muscle metabolism in exercise physiology.,,,, Nevertheless, accessibility and cost limit the development of the technique for exercise investigations. Last, it is not possible to measure the moving leg during walking.
Using muscle scintigraphy allows for the evaluation of muscle blood flow but does not analyze oxygen pressure in the muscle., The ability of scintigraphy to estimate the perfusion segment by segment and differentiate buttock from the thigh from calf perfusion is clearly of interest.,,,, Accessibility, cost, and irradiation all remain limitations of this tool that can mainly remain a research technique.
| Indications for Exercise-Transcutaneous Oxygen Pressure Measurement in Patients with Claudication|| |
Calf pain can be caused by nonvascular diseases, such as neurologic claudication, sciatica or neuromuscular, or osteoarticular symptoms. Further, isolated proximal–noncalf-ischemia can explain a normal calf TcPO2 result but can induce pain involving the calf. A specific interest of the technique is the estimation of abnormal perfusion in areas that are hardly accessible to ultrasound recording (buttock circulation).,,, A second interest is the detection of systemic hypoxemia as a potential cause of walking impairment associated with PAD.,,, Nevertheless no evidence exists to date that Ex-TcpO2 participates in a better outcome of detected patients. The last situation of specific interest is the patients with uncompressible arteries where ABI postexercise cannot be performed (i.e., diabetic patients or patients with renal failure that are at high risk of lower limb vascular calcifications). The results of exercise oximetry in diabetic versus nondiabetic patients  show that patients with diabetes show more severe limitation on the treadmill and more nonlimb symptoms, and more distal ischemia than patients without diabetes, with no difference at the buttock level.
| Trics and Traps for Doing an Exercise Transcutaneous Recording|| |
The method proposed to perform an exercise oximetry test has been largely described elsewhere., The following items are only some keypoints to guide potential users that would start developing the technique.
- Avoid cold environment. The room temperature should be at least 22°C
- Calibration of probes to air should be performed at least twice before each test
- Avoid hairs or carefully shave the skin before attaching the fixing rings
- Dry the skin eventually with ether to improve ring adherence
- Do not completely fill the probe holder with contact liquid
- Avoid area of concavity and tendons to limit the risk of disconnection
- Any value above 100 mmHg is suspect of probe disconnection
- Use a chest reference electrode and at least one (or multiple) peripheral probes
- Wait for at least 15 min once the probes are on the patient to allow local heating
- Record 1 (ideally 2) min at rest for the calculation of DROP
- Record a minimum of 5 (ideally 10) min of postexercise recovery
- Check for electronic drift after the test by checking posttest air value
- Always check the chest changes when interpreting DROP results.
| Questions for the Future|| |
Typical examples of exercise oximetry results are reported in [Figure 3]a,[Figure 3]b,[Figure 3]c. Many points still need to be clarified about the use of exercise oximetry. Among these: the cost-effectiveness of the technique; the position among other tools in the diagnostic algorithm of exertional limb pain of suspected vascular origin; the definition of the population that should undergo this procedure.
|Figure 3: Typical original example of recordings with 8 probes. The period of exercise (“Phase d'effort”) is in gray rectangle starting at min 2. The left chest (“Thorax G”) reference changes are presented on the upper panels of each figure. On lower panels, “Fesse gauche” stands for left buttock (dark blue), “Cuisse gauche” stands for left thigh (pink), “Jambe gauche” stands for left calf (yellow), “Fesse droite” stands for right buttock (Green), “Cuisse droite” stands for right thigh (Light blue), and “Jambe droite” stands for right calf (Red); Note that the black line on the lower panels are the right chest (“Thorax D”) probe expressed as a delta from rest of oxygen pressure. Logically, delta from rest of oxygen pressure of the second chest is approximately zero confirming that the two chest probes had similar changes throughout the test. Horizontal redline is the normal limit used for analysis (−15 mmHg). Vertical redline is event markers corresponding to pain occurrence. (a) bilateral distal ischemia. Proximal ischemia is also significant except on the left thigh. (b) significant but nonlimiting ischemia of the right thigh, right calf and to a lesser degree right buttock. (c) significant ischemia of the left calf but occurring only during the recovery period. The specific interest here is the decrease of chest transcutaneous oxygen pressure measurement during exercise that we interpret as limiting exercise-induced systemic hypoxemia|
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| Conclusion|| |
On the one hand in medicine, physicians cannot satisfy of the presence of a lesion at rest to claim that this lesion is responsible for the symptomatology of the patients. In PAD patients, it is well known that patients with femoral occlusion may remain perfectly asymptomatic and not only because of the absence of physical activity. On the other hand, nobody would accept that chest angina is excluded on the basis of a normal resting electrocardiogram. As in any exercise-related disease, a resting normal Doppler and a resting ABI within the normal limits should not lead to the conclusion that the lower limb symptoms are not of arterial origin. Finally, the frequent situations where comorbid conditions coexist in the same patient questioning which disease is the principal responsible for the patient complains of walking impairment.
The technique is simple and can be performed by a technician or a nurse under medical supervision but remains time-consuming. In our opinion, diagnostic exercise testing in general, and diagnostic exercise oximetry specifically remain largely underused and when performed, significantly impacts patient care. Claudication is an exercise-related symptom and relying on resting investigation to diagnose and evaluate patients suffering lower limb exertional pain should no longer be the dominant practice.
The authors would like to thank I; Laporte and M Feuilloy for technical help.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3]