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Table of Contents
ORIGINAL ARTICLE
Year : 2018  |  Volume : 1  |  Issue : 3  |  Page : 93-97

Near-infrared spectroscopy of the thigh fails to discriminate cyclists with arterial endofibrosis from normal asymptomatic athletes


1 Department of Sports Medicine, University Hospital of Angers, Angers, France
2 Department of Vascular and Thoracic Surgery, University Hospital of Angers, Angers, France
3 Department of Vascular Medicine, University Hospital of Angers, Angers, France
4 Department of Sports Medicine; Department of Vascular Medicine, University Hospital of Angers; Research Unit, INSERM 1083-CNRS 6015, Mitovasc Institute, Angers, France

Date of Web Publication30-Apr-2019

Correspondence Address:
P Abraham
Department of Sports Medicine, University Hospital of Angers, 4 Larrey Street, 49100 Angers
France
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/VIT.VIT_1_19

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  Abstract 

BACKGROUND: This study is to assess the applicability and performance of the near-infrared spectroscopy (NIRS) in the diagnosis of exercise-induced arterial endofibrosis (EIAE).
METHODS: NIRS was measured on each thigh, in 12 highly trained asymptomatic cyclists (controls) and 14 EIAE patients highly trained competition cyclists. All patients had an incremental bicycle stress test until exhaustion or symptom limitation. Results are presented as median (25°; 75° centiles) and between groups difference calculated with Mann–Whitney test.
RESULTS: Six of the NIRS recordings technically failed: three in controls and three in EIAE patients due to probe disconnection. In the remaining nine controls and 11 EIAE patients, no difference was found at peak exercise for tissue saturation index (−2.0% [−8.5; 2.1] vs. −4.0% [−5.9; 5.5]; P = 0.710) or for half-time recovery (42.0 s [24.9; 105.0] vs. 42.0 s [33.0; 112.7]; P = 0.905) between EIAE and controls, respectively.
CONCLUSION: NIRS, when available, does not satisfactorily discriminate patients with EIAE from asymptomatic healthy athletes.

Keywords: Diagnostic method, endurance sports, exercise-induced arterial endofibrosis, incremental test, near-infrared spectroscopy


How to cite this article:
Julienne T, Ammi M, Hersant J, Henni S, Abraham P. Near-infrared spectroscopy of the thigh fails to discriminate cyclists with arterial endofibrosis from normal asymptomatic athletes. Vasc Invest Ther 2018;1:93-7

How to cite this URL:
Julienne T, Ammi M, Hersant J, Henni S, Abraham P. Near-infrared spectroscopy of the thigh fails to discriminate cyclists with arterial endofibrosis from normal asymptomatic athletes. Vasc Invest Ther [serial online] 2018 [cited 2019 Jul 20];1:93-7. Available from: http://www.vitonline.org/text.asp?2018/1/3/93/257413


  Introduction Top


Exercise-induced arterial endofibrosis (EIAE) mainly affects young men without cardiovascular risk factor. It is histologically characterized by a fibrous thickening of the endothelial and medial wall of the artery, resulting in a reduction of the diameter of the lumen.[1],[2],[3] Once suspected, the diagnosis is strengthened by the presence of a vascular bruit in iliac fossa and a decrease in ankle to brachial index (ABI). The normal limit to define an abnormal ABI response remains debated.[4] Ultrasound imaging can provide further arguments for endofibrosis but remains difficult, even in trained hands. Finally, radiological imaging is invasive and should only be proposed when surgery is decided and when the diagnosis is already confirmed (or at least strongly suspected) with noninvasive tests.[5],[6],[7]

Near-infrared spectroscopy (NIRS) is rapidly spreading in the field of sports or vascular medicine. The technique is not invasive, nonirradiating, assumed to measure muscle oxygenation and allows measurements in motion. This last point is essential and theoretically very advantageous over postexercise (ABI or ultrasound) measures. Some studies have shown variations of deep tissue oxygenation in athletes,[8],[9],[10] but the diagnostic performance of NIRS in EIAE has never been tested. We hypothesized that NIRS-derived parameters could discriminate EIAE from normal asymptomatic athletes.


  Materials and Methods Top


We performed a prospective study in the Service of Sports Medicine of the University Hospital of Angers, between November 2014 and February 2016. Eligible individuals were highly trained competition cyclists referred for bicycle stress tests either for a systematic follow-up of exercise performance (controls) or for suspicion of endofibrosis (EIAE). Inclusion criteria were: Age between 18 and 40 years old. Patients with EIAE suspicion were included only if fulfilling all three following clinical criteria: unilateral exercise-induced pain by history and on laboratory bicycle, postexercise ABI ≤0.65 on the painful side, presence of an intense postexercise iliac bruit on the symptomatic side. Patients with only one or two criteria were excluded as well as individuals with bilateral lower limb exercise-related symptoms. Finally, we searched for the results of histology on follow-up, for the patients of EIAE group that underwent surgery to confirm EIAE. Patients of the control group were strictly asymptomatic and had none of the clinical criteria.

Written and signed consent to participate to the study after clear information was obtained from all patients. This study conformed to the principles of the declaration of Helsinki and was registered under reference NCT02501694 in www.clinicaltrial.gov.

The NIRS recording began with a resting phase of 2 min in the recumbent position. Thereafter, patients were installed on their own bicycle positioned on a cycle ergometer (CYCLUS2, RBM elektronik-automation GmbH, Germany) to reproduce the best field conditions. Thereafter, athletes performed a maximal exercise test using an incremental workload protocol by steps of 50 watts every 2 min up to 300 watts and 30 watts increments thereafter, until exhaustion. At maximal exercise, athletes were asked to lie in the recumbent position again for passive recovery.

Throughout rest, exercise, and recovery, we recorded NIRS with a sample rate of 10 Hertz on both sides with a two channels system (Portalite®, Artinis Medical Systems, NL). Sensors were placed symmetrically on the front right and left quadriceps, mid-thigh. As shown in [Figure 1], probes were fixed to the side with double side adhesives and stabilized with a net around the thigh to decrease the risk of disconnection during exercise. The system provides the following parameters:
Figure 1: Near infra-red spectroscopy sensor with double-sided adhesives around the emitting diodes and receptors. Note the position of the sensor on the thigh and the presence of the net to stabilize the probe

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  • The oxygenated hemoglobin, or OXY-hemoglobin (O2Hb; micro-mol/L)
  • The deoxygenated hemoglobin or the deoxyhemoglobin (HHb; micro-mol/L)
  • The total hemoglobin (tHb; micro-mol/L)
  • The tissue saturation index (TSI; %).


Statistical analysis

The NIRS recordings were analyzed using the Excel software and BIOPAC. Smoothing averaging over 10 consecutive values was performed from raw data to decrease the instantaneous variability. From recording of TSI, we calculated Half time recovery (T1/2; sec), assumed to be higher in the presence than in the absence of ischemia. Last, for all other parameters, resting values (rest) are reported as the average over 2 min of the resting period. Peak exercise values (peak) are the average of the last 2 min of exercise.

We compared the EIAE leg to the lowest O2Hb, tHb, TSI and highest HHb and T1/2 value of controls and the asymptomatic limb of patients to highest O2Hb, tHb, TSI, and lowest HHb and T1/2 value of controls. In EIAE patients with unilateral symptoms, we compared to the difference between the symptomatic minus asymptomatic limb of EAIE patient with the difference between the left minus right limb, of control patients.

Results are reported as mean ± standard deviation for age and body mass index and between limb differences and as median with (25°; 75° centiles) for NIRS absolute parameters. Between groups comparison for NIRS derived parameters was performed by the nonparametric Mann–Whitney test. For all recorded values, a receiver operating characteristic (ROC) Curve analysis was performed with the comparison of the area to the random choice (Area 0.50). P ≤ 0.05 for Mann-Whitney test was taken as statistically significant. Statistical analyses were performed with SYSTAC 13.0.1 (Systat Inc., USA).


  Results Top


Population

Thirty-two patients agreed to participate and gave their consent for inclusion. Six patients had bilateral symptoms or only one or two clinical criteria after exercise and were excluded. The included individuals consisted of 12 patients for the control group (26.0 ± 5.1 years and 22.1 ± 1.0 kg/m2) of 14 patients for the EIAE group (26.0 ± 4.2 years; 21.0 ± 1.0 kg/m2). All included patients were involved in regular training for a variable level of competition (from regional to international). Among included individuals, no patient was under medical treatment. No risk factors for arterial disease were noted in any of the AIAE or control patients. Patients with EIAE had a history of limb exercise-related symptoms for 3 months–3 years.

Feasibility

Six of the NIRS recordings were technically incomplete: three in the control group and three in EIAE group. This represents 18.8% of the recordings performed. In most cases, the reason was the disconnection of the probe from the skin despite the adhesive and presence of the net around the thigh to stabilize the probes. In one case, this was due to a failure in the transmission between probes and the recording computer.

Near-infrared spectroscopy analysis

The finally studied individuals with available NIRS results consisted of nine patients for the control group of 11 patients for the EIAE group. Nine of the 11 EIAE patients underwent surgery with the diagnosis confirmed in all operated cases by histological findings. One patient refused surgery, and one patient was lost on follow-up.

An example of TSI recording of the EIAE group is displayed in [Figure 2] (EIAE is left side). Although the absolute value was slightly lower on the affected side both at rest and during exercise, the changes over time and decrease are comparable to those observed in the controls. Results for the different NIRS derived parameters at rest and peak exercise and for T1/2 are reported in [Table 1]. As shown, no significant difference was found for any of the studied parameters, specifically for peak TSI: 57.7% (53.1; 64.3) that on average trended to be even higher than the lowest values observed in the lowest leg of controls: 50.7% (47.7; 57.0): P = 0.456. As a logical result, area under ROC curves ranged from 0.517 ± 0.138 for T1/2 to 0.722 ± 0.118 for HHB at rest with nonsignificant P values (difference from 0.50) ranging from 0.903 to 0.102, respectively. Similarly, there was no difference in the half time recovery between these two groups. Results for the between-limb differences reported in [Table 2] also show no difference between EIAE patients and normal controls. As a logical result, the area under ROC curves ranged from 0.500 ± 0.144 for Peak TSI to 0.713 ± 0.135 for Peak O2Hb with nonsignificant P values (difference from 0.50) ranging from 1.000 to 0.131, respectively.
Figure 2: Example of tissue saturation index curve (expressed in %) for an athlete of the exercise-induced arterial endofibrosis group (pathological left side). D_tissue saturation index is for right thigh value, G_tissue saturation index is for left side value. The exercise period starts at minute 2 and ends at minute 17

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Table 1: Absolute value for the asymptomatic and symptomatic leg in exercise-induced arterial endofibrosis and lowest and highest leg in controls

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Table 2: Difference of asymptomatic minus symptomatic leg in exercise-induced arterial endofibrosis and right minus left leg in controls

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  Discussion Top


Although NIRS is assumed to detect exercise-induced ischemia, during exercise, beyond technical and practical issues, contrary to our hypothesis and expectations, NIRS did not differentiate EIAE from control athletes.

From the literature, the TSI and T1/2 are the parameters that seem most relevant in NIRS recordings to discriminate between normal individuals and claudicants.[11],[12] NIRS is expected to measure muscle oxygenation although previous reports has shown the dramatic influence of skin blood flow over NIRS results.[13] Endofibrosis being an exercise-induced disease, significant TSI decrease at peak exercise and/or T1/2 increase in EIAE as compared to controls were expected. Although the absence of significance might be due to the limited power of our study as further discussed below, the P values are far from significance. It should be noted that the left minus right limb difference in controls was preferred to the comparison of lowest minus highest value to increase the chance to observe a difference in EIAE patients compared to controls.

The high standard deviations observed in the control group when comparing the two legs seem inconsistent with the previously reported satisfactory reliability of NIRS measurements.[14] In these completely asymptomatic patients, we doubt that this could be due to unknown EIAE but it cannot be excluded, and systematic invasive imaging to try to further exclude minor unknown lesions was not ethically acceptable. This variability may also possibly be explained by a dominant leg of cycling not considered in this study, and laterality is a potential bias.

First, various NIRS devices are available on the market and use different algorithms different wavelengths and different filters of the signal,[15],[16],[17] and different emitter to transmitter distances.[18] Then, whether or not different NIRS devices would result in the same results is unsure and a limitation of our study. Second, the quadriceps muscle may be not the optimal position for the probes. Nevertheless, usual symptoms in EIAE are located in the thigh.[3] Third, going from the standing to the lying position may have possibly interfered with NIRS results, but postexercise ABI cannot be attained in the standing position during the recovery phase. Unfortunately, most patients coming to our laboratory were not able to return for a second series of tests due to distance from home, and repeating the maximal test immediately was hardly acceptable and might have resulted in a long-lasting effect of the first tests over the results of the second one. Finally, the number of individuals recruited is small, and the study possibly lack power to definitively exclude NIRS as a potential tool for EAIE diagnosis. Nevertheless, based on the results of this pilot study, each group of indididuals would have to be ~ 200 individuals to reach statistical significance while all published studies to date are isolated case report or very small series of cases. Then, even positive for such a high number of studied patients the interest at the individual level would be debatable.


  Conclusion and Perspectives Top


This pilot study suggests that NIRS using Portalite®, does not satisfactorily discriminate patients with EIAE from asymptomatic healthy athletes. All these observations call for future development of simple and accurate diagnostic tests for EIAE screening and for research studies on the physiopathology of this disease.

Acknowledgment

The authors thank the “direction de la recherche clinique” for technical support and the SOCOS group.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Shalhub S, Zierler RE, Smith W, Olmsted K, Clowes AW. Vasospasm as a cause for claudication in athletes with external iliac artery endofibrosis. J Vasc Surg 2013;58:105-11.  Back to cited text no. 1
    
2.
Moumouni I, Anthony AD, Matysiak L. Thrombosis of external iliac artery due to endofibrosis. Arch Cardiovasc Dis 2014;107:142-3.  Back to cited text no. 2
    
3.
Feugier P, Chevalier JM. Endofibrosis of the iliac arteries: An underestimated problem. Acta Chir Belg 2004;104:635-40.  Back to cited text no. 3
    
4.
INSITE Collaborators (INternational Study group for Identification and Treatment of Endofibrosis). Diagnosis and management of iliac artery endofibrosis: Results of a delphi consensus study. Eur J Vasc Endovasc Surg 2016;52:90-8.  Back to cited text no. 4
    
5.
Alimi YS, Accrocca F, Barthèlemy P, Hartung O, Dubuc M, Boufi M. Comparison between duplex scanning and angiographic findings in the evaluation of functional iliac obstruction in top endurance athletes. Eur J Vasc Endovasc Surg 2004;28:513-9.  Back to cited text no. 5
    
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Giannoukas AD, Berczi V, Anoop U, Cleveland TJ, Beard JD, Gaines PA. Endofibrosis of iliac arteries in high-performance athletes: Diagnostic approach and minimally invasive endovascular treatment. Cardiovasc Intervent Radiol 2006;29:866-9.  Back to cited text no. 6
    
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Peach G, Schep G, Palfreeman R, Beard JD, Thompson MM, Hinchliffe RJ. Endofibrosis and kinking of the iliac arteries in athletes: A systematic review. Eur J Vasc Endovasc Surg 2012;43:208-17.  Back to cited text no. 7
    
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Jones B, Hesford CM, Cooper CE. The use of portable NIRS to measure muscle oxygenation and haemodynamics during a repeated sprint running test. Adv Exp Med Biol 2013;789:185-91.  Back to cited text no. 8
    
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Hesford CM, Laing S, Cooper CE. Using portable NIRS to compare arm and leg muscle oxygenation during roller skiing in biathletes: A case study. Adv Exp Med Biol 2013;789:179-84.  Back to cited text no. 9
    
10.
Ruan ZS, Li T, Ren RR, Zhao Y, Li K, Mao YF, et al. Monitoring tissue blood oxygen saturation in the internal jugular venous area using near infrared spectroscopy. Genet Mol Res 2015;14:2920-8.  Back to cited text no. 10
    
11.
Alfonsi E, Pavesi R, Merlo IM, Gelmetti A, Zambarbieri D, Lago P, et al. Hemoglobin near-infrared spectroscopy and surface EMG study in muscle ischaemia and fatiguing isometric contraction. J Sports Med Phys Fitness 1999;39:83-92.  Back to cited text no. 11
    
12.
Vardi M, Nini A. Near-infrared spectroscopy for evaluation of peripheral vascular disease. A systematic review of literature. Eur J Vasc Endovasc Surg 2008;35:68-74.  Back to cited text no. 12
    
13.
Davis SL, Fadel PJ, Cui J, Thomas GD, Crandall CG. Skin blood flow influences near-infrared spectroscopy-derived measurements of tissue oxygenation during heat stress. J Appl Physiol (1985) 2006;100:221-4.  Back to cited text no. 13
    
14.
Buchheit M, Ufland P, Haydar B, Laursen PB, Ahmaidi S. Reproducibility and sensitivity of muscle reoxygenation and oxygen uptake recovery kinetics following running exercise in the field. Clin Physiol Funct Imaging 2011;31:337-46.  Back to cited text no. 14
    
15.
Matcher SJ, Elwell CE, Cooper CE, Cope M, Delpy DT. Performance comparison of several published tissue near-infrared spectroscopy algorithms. Anal Biochem 1995;227:54-68.  Back to cited text no. 15
    
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Boushel R, Piantadosi CA. Near-infrared spectroscopy for monitoring muscle oxygenation. Acta Physiol Scand 2000;168:615-22.  Back to cited text no. 16
    
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Denault A, Deschamps A, Murkin JM. A proposed algorithm for the intraoperative use of cerebral near-infrared spectroscopy. Semin Cardiothorac Vasc Anesth 2007;11:274-81.  Back to cited text no. 17
    
18.
Koga S, Barstow TJ, Okushima D, Rossiter HB, Kondo N, Ohmae E, et al. Validation of a high-power, time-resolved, near-infrared spectroscopy system for measurement of superficial and deep muscle deoxygenation during exercise. J Appl Physiol (1985) 2015;118:1435-42.  Back to cited text no. 18
    


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2]



 

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