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Intra- and Inter-rater Reliability of Peripheral Arterial Blood Flow Velocity by Means of Doppler Ultrasound
Intra- and Inter-rater Reliability of Peripheral Arterial Blood Flow Velocity by Means of Doppler Ultrasound Elaine Caldeira de Oliveira Guirro, PT, PhD, Gabriella de Paula Marcondes Ferreira Leite, PT, Almir Vieira Dibai-Filho, PT, Nathalia Cristina de Souza Borges, PT, and Rinaldo Roberto de Jesus Guirro, PT, PhD ABSTRACT Objective: Although it is possible to find studies that analyze the velocity of blood flow in different arteries, the reliability of Doppler ultrasound on peripheral arteries has not yet been completely established. Our objective was to evaluate intra- and inter-rater reliability of the measurement of blood flow velocity by Doppler ultrasound of brachial, radial, popliteal, and posterior tibial arteries. Methods: Fifty healthy individuals of both genders, aged between 18 and 45 years, were included in the study. For the evaluation of arterial blood flow velocity, a portable Doppler ultrasound device was used to measure the mean and maximum blood flow velocity of posterior tibial, popliteal, brachial, and radial arteries. Two examiners performed assessments of the same volunteers independently and twice, with an interval of 1 week between them. Results: We found good to very good reliability for measuring the mean and maximum blood flow velocity of the arteries evaluated. The intraclass correlation coefficients ranged between 0.501 and 0.866, standard error of measurement ranged between 0.81 and 9.45 cm/s, and minimum detectable change ranged between 2.25 and 26.13 cm/s. Conclusion: The assessment of mean and maximum blood flow velocity of the brachial, radial, popliteal, and posterior tibial arteries by means of Doppler ultrasound presents acceptable reliability values, which supports the use of this evaluation method in research and clinical practice. (J Manipulative Physiol Ther 2017;40:236-240) Key Indexing Terms: Blood Flow Velocity; Reproducibility of Results; Arteries
INTRODUCTION The evaluation of peripheral blood flow is extremely important in clinical practice for the diagnosis of circulatory system changes. 1 The decrease in the blood flow velocity indicates a reduction in the caliber of the vessels, which may suggest the occurrence of stenosis or vascular lumen obstruction. 2 In this sense, determining the blood flow velocity of peripheral arteries is a procedure that has been employed with various purposes, such as the detection of peripheral artery Postgraduate Program in Rehabilitation and Functional Performance, Department of Biomechanics, Medicine, and Rehabilitation of the Locomotor Apparatus, Medical School of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil. Corresponding author: Elaine Caldeira de Oliveira Guirro, PT, PhD, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Curso de Fisioterapia, Avenida dos Bandeirantes, 3900, Monte Alegre, Ribeirão Preto, SP, Brasil, CEP 14049-900. (e-mail: [email protected]). Paper submitted August 25, 2015; in revised form November 18, 2015; accepted April 5, 2016. 0161-4754 Copyright © 2017 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2017.02.007
diseases; classification of the risk of a patient developing ulcers, gangrene, and amputation 3; diagnosis of circulatory dysfunctions after surgeries 2,4; and assessment of effects of the therapeutic resources on blood circulation. 5,6 Doppler ultrasound is a noninvasive method for the evaluation of blood circulation. The transducer is placed on the site to be evaluated using gel as a conductor, with an approximate angle of 30°, and the ultrasonic waves are emitted and projected obliquely to the blood flow, being reflected by erythrocytes and producing spectral analysis and calculation of the hematological profile found. 7 Although Doppler ultrasound is widely used for this purpose, it is known that absolute measurements of arterial blood flow depend on several factors, such as the examiner, patient, equipment, protocols, and environment of application. 4,8,9 Even considering a possible variability of results, few studies have focused on reliability and reproducibility of the blood flow velocity variable identified by the Doppler ultrasound device. However, studies on hepatic, 10 ophthalmic, 11 uterine, 12 and brain 13 arteries reveal that, with standardization of evaluations, Doppler ultrasound has good reliability of results, both in terms of the time and examiners. Based on these considerations, and although studies have investigated the behavior of the blood flow in different
Journal of Manipulative and Physiological Therapeutics Volume 40, Number 4
arteries, such as the brachial, 14 femoral, 15 and popliteal, 16 the reliability of Doppler ultrasound on peripheral arteries has not yet been completely established. Thus, the present study aimed to evaluate the intra- and inter-rater reliability of the measurement of the blood flow velocity by means of Doppler ultrasound in the brachial, radial, popliteal, and posterior tibial arteries. The hypothesis of this study was that the evaluation of blood flow velocity has acceptable reliability values for its use in research and in clinical settings.
METHODS Sample The sample size was based on the guidelines for the evaluation of measurement properties, 17 in which at least 50 participants would be necessary to evaluate the reproducibility and validity of the construct. 18 Thus, 51 volunteers were recruited by means of verbal invitation and posters in the university community of Ribeirão Preto (SP, Brazil). In this study, we included volunteers without health issues that could compromise analyses (healthy individuals) of both genders and aged between 18 and 45 years. As exclusion criteria, we adopted the presence of circulatory or metabolic diseases, systemic diseases that affect the circulatory system, neurologic or neuromuscular diseases, use of drugs that affect the circulatory system, and treatment with physical therapy or physical activity during the data collection period. In the face of these eligibility criteria, there was sample loss of 1 volunteer as a result of nonattendance in the second session, and thus the final sample was composed of 50 individuals. This study was approved by the Research Ethics Committee of Clinics Hospital of the Medical School of Ribeirão Preto of the University of São Paulo under protocol number 313882/2013.
Doppler Ultrasound For the evaluation of arterial blood flow velocity, a portable Doppler device SONAR/tek (Nicolet Vascular, Natus, San Carlos, CA) was used with spectral analysis and data about components of the flow profile. The volunteers were examined after 10 minutes of rest in the dorsal decubitus position in an air-conditioned room at 23°C and humidity of 50%. The evaluations were performed in dominant lower and upper limbs. Two examiners captured Doppler signals from posterior tibial and radial arteries with a probe of 8 MHz and from popliteal and brachial arteries with a probe of 4 MHz, which were used as a parameter the mean and maximum velocity of the arterial blood flow (in cm/s). Three collections for each artery (each windowing with 10 seconds) were carried out, considering the mean for statistical calculations. The order to measure the arteries was randomized.
Guirro et al Reliability of Doppler Ultrasound
Evaluation Procedure Signal processing was performed with SONARA/tek software, considering the entire period of collection. The evaluations of velocity in arteries were conducted by 2 examiners previously trained in use of the Doppler ultrasound. The examiners performed evaluations with the same volunteers independently and twice, with an interval of 1 week between them, 19 thus enabling the measurement of intra- and inter-rater reliability.
Statistical Analysis The intraclass correlation coefficient (ICC3,2) was used to determine the intra- and inter-rater reliability, with their respective 95% confidence intervals, standard errors of measurement (SEM), and minimum detectable change (MDC), according to Tucci et al. 20 The interpretation of ICC values was based on that suggested by Weir. 21 For values ranging from 1.00 to 0.81, the reliability was considered excellent; from 0.80 to 0.61, very good; from 0.60 to 0.41, good; from 0.40 to 0.21, reasonable; and finally, from 0.20 to 0.00, poor. All the statistical analysis was performed using the Statistical Package for Social Sciences software, version 17.0 (SPSS Inc., Chicago, IL).
RESULTS The sample of the present study was composed of 50 individuals of both genders (40 women, 10 men) and 43 righthanders, with mean age of 25.10 years (standard deviation [SD] = 4.18) and mean body mass index of 22.89 kg/m 2 (SD = 3.72). The values of mean and maximum velocity of arterial blood flow obtained by both examiners are described in Table 1. Table 2 presents the values of intrarater reliability from the measurement of mean velocity of arterial blood flow, and good to very good reliability was noted, with ICC values ranging between 0.510 and 0.722, SEM values ranging between 1.17 and 2.67 cm/s, and MDC values ranging between 3.25 and 7.37 cm/s. With regard to the inter-rater reliability from the measurement of mean velocity of arterial blood (Table 3), very good reliability was noted, with ICC values ranging between 0.700 and 0.780, SEM values ranging between 0.81 and 2.10 cm/s, and MDC values ranging between 2.55 and 5.82 cm/s. The values of intrarater reliability from the measurement of maximum velocity of arterial blood flow are in Table 4. Good to very good reliability was noted, with ICC values ranging between 0.539 and 0.659, SEM values ranging between 3.80 and 9.41 cm/s, and MDC values ranging between 10.50 and 26.13 cm/s. With regard to the inter-rater reliability from the measurement of maximum velocity of arterial blood (Table 5), good to very good reliability was noted, with ICC values ranging between 0.595 and 0.866, SEM values ranging
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Journal of Manipulative and Physiological Therapeutics May 2017
Table 1. Description of Values of Mean and Maximum Velocity of Arterial Blood Flow (in cm/s) Obtained by Both Examiners Blood Flow
Artery
Examiner 1
Examiner 2
Test
Retest
Test
Retest
Brachial
Mean Maximum
13.28 (3.99) 59.03 (10.54)
12.92 (3.16) 57.07 (9.55)
11.49 (3.78) 52.28 (11.51)
12.41 (4.52) 54.53 (14.27)
Radial
Mean Maximum
4.09 (1.86) 23.88 (6.06)
3.99 (1.21) 24.67 (5.31)
4.36 (2.14) 25.70 (6.96)
4.38 (1.62) 26.57 (7.71)
Popliteal
Mean Maximum
8.52 (3.59) 38.90 (16.28)
8.46 (3.40) 38.11 (14.99)
7.72 (3.41) 35.20 (12.49)
7.99 (3.99) 34.45 (14.69)
Posterior tibial
Mean Maximum
4.86 (2.14) 27.00 (9.20)
4.63 (1.82) 26.76 (8.08)
5.45 (3.43) 28.23 (10.17)
5.06 (2.17) 28.95 (7.97)
Values shown as mean (standard deviation).
Table 2. Intrarater Reliability of the Measurement of Mean Blood Flow Velocity of Peripheral Arteries With Doppler Ultrasound
Table 3. Inter-rater Reliability of the Measurement of Mean Blood Flow Velocity of Peripheral Arteries With Doppler Ultrasound
Artery
ICC
95% CI
SEM
MDC
Artery
ICC
95% CI
SEM
MDC
Brachial Radial Popliteal Posterior tibial
0.519 0.520 0.501 0.722
0.153, 0.727 0.153, 0.727 0.120, 0.717 0.510, 0.842
2.67 1.17 2.53 1.63
7.37 3.25 7.00 4.53
Brachial Radial Popliteal Posterior tibial
0.702 0.769 0.780 0.700
0.474, 0.831 0.592, 0.869 0.613, 0.875 0.472, 0.830
2.10 0.81 1.68 1.70
5.82 2.25 4.65 4.70
CI, confidence interval; ICC, intraclass correlation coefficient; MDC, minimum detectable change (in cm/s); SEM, standard error of measurement (in cm/s).
CI, confidence interval; ICC, intraclass correlation coefficient; MDC, minimum detectable change (in cm/s); SEM, standard error of measurement (in cm/s).
between 2.98 and 8.14 cm/s, and MDC values ranging between 8.25 and 22.51 cm/s.
peripheral arteries, including the establishment of the standard error of measurement and minimum detectable change. Thus, our study presents this uniqueness and identified ICC values lower than Guirro et al. 6 However, according to the reference established by Weir, 21 good to very good reliability was identified in the present study, with intrarater ICC raging between 0.501 and 0.722 and inter-rater ranging between 0.595 and 0.866. In this context, Osada 27 reported intrarater ICC values of 0.94, 0.90, and 0.85 for the blood flow of the abdominal aortic, left femoral, and right femoral arteries, respectively. Billinger and Kluding 28 reported intra-rater ICC values of 0.96 and 0.98 for the measurement of femoral blood flow velocity of the hemiparetic and nonhemiparetic limbs, respectively, in people with stroke. In their turn, McDonnell et al 29 evaluated the blood flow velocity of intracranial arteries in different positions and obtained intrarater ICC values of 0.822 for the seated volunteers and 0.734 for the lying volunteers and inter-rater ICC values of 0.504 for sitting and 0.081 for the lying position. However, comparisons between our study and the previously mentioned investigations must be made with caution, given that anatomic location influences reliability, although all of them recommend Doppler ultrasound for the evaluation of arterial blood flow. Other authors have evaluated the reliability of measuring the blood flow velocity of veins. Crisóstomo et al 30 evaluated the intrarater reliability of peak blood flow velocity of the popliteal vein in patients with primary chronic venous disease by means of Doppler ultrasound at baseline and during 3 sets of 10 tiptoe movement repetitions and noted that the reliability
DISCUSSION Good to very good reliability for the measurement of mean and maximum velocity of blood flow in the posterior tibial, popliteal, brachial, and radial arteries by means of Doppler ultrasound was identified in the present study. It is worth noting the recent focus of several studies on this property of instruments of biological signals assessment. 22-24 Complementing and highlighting the importance of investigations on the topic of this study, Kottner et al 25 observed that results of reliability and agreement studies provide information about the amount of error inherent in any diagnosis, score, or measurement, where the amount of measurement error determines the validity of the study results or scores. Although previous studies have investigated the behavior of blood flow velocity of peripheral arteries in diverse populations, 2,15,26 the scientific literature provides scarce information on the reliability of Doppler ultrasound in these arteries. Only the crossover clinical trial conducted by Guirro et al. 6 performed the analysis of intrarater reliability of the maximum blood flow velocity as a complement to the data analysis and found an ICC value of 0.796 for popliteal artery and ICC value of 0.899 for posterior tibial artery. The study in question did not evaluate arteries of the upper limb. Moreover, the authors suggested that future studies should be developed focusing on the intra- and inter-rater reliability in various
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Guirro et al Reliability of Doppler Ultrasound
Table 4. Intrarater Reliability of the Measurement of Maximum Blood Flow Velocity of Peripheral Arteries With Doppler Ultrasound Artery
ICC
95% CI
SEM
MDC
Brachial Radial Popliteal Posterior tibial
0.539 0.659 0.581 0.602
0.187, 0.738 0.399, 0.806 0.262, 0.762 0.299, 0.774
7.78 3.80 9.45 5.58
21.50 10.50 26.13 15.42
CONCLUSION The assessment of mean and maximum blood flow velocity of brachial, radial, popliteal, and posterior tibial arteries by means of Doppler ultrasound presents acceptable reliability values, which supports the use of this evaluation method in research and clinical practice.
CI, confidence interval; ICC, intraclass correlation coefficient; MDC, minimum detectable change (in cm/s); SEM, standard error of measurement (in cm/s).
FUNDING SOURCES
Table 5. Inter-rater Reliability of the Measurement of Maximum
No funding sources or conflicts of interest were reported for this study.
Blood Flow Velocity of Peripheral Arteries With Doppler Ultrasound Artery
ICC
95% CI
SEM
MDC
Brachial Radial Popliteal Posterior tibial
0.595 0.702 0.689 0.866
0.287, 0.770 0.476, 0.831 0.451, 0.823 0.764, 0.924
7.29 3.55 8.14 2.98
20.15 9.82 22.51 8.25
CI, confidence interval; ICC, intraclass correlation coefficient; MDC, minimum detectable change (in cm/s); SEM, standard error of measurement (in cm/s).
of peak blood flow velocity was high (ICC = 0.70) for values obtained in the first contraction of the set but lowered when using the last contraction (ICC b 0.50). In addition to this study, Fernandez et al 31 found values of intra- and inter-rater ICC of 0.59 and 0.46, respectively, when measuring the maximum blood flow velocity of the umbilical vein. In these terms, although the arterial and venous blood flows have distinct features, such as vessel structure, anatomic location, and flow type, the results of these investigations are similar to that of our study, in which most of ICC values were between 0.501 and 0.780. The description of SEM and MDC values was not found in studies of the literature that focused on the reliability of measurement of blood flow velocity by Doppler ultrasound. In current times, these 2 indicators are necessary for studies that evaluate reliability. SEM indicates errors during the measurement of a particular variable with an evaluative tool; in other words, it is an indication of the precision of a score. 21 With regards to MDC, Tucci et al 20 highlighted that it is important to have knowledge about the minimal difference in the scores of an evaluation tool between revaluation sessions that could be considered a real improvement with no error. Therefore, we suggest that future studies should implement the calculation of SEM and MDC in their statistical analysis to establish error parameters in measurements. The calculation of the Doppler ultrasound reliability was conducted in healthy participants, which is common in other published investigations. 19,32,33 However, we emphasize that the presence of diseases that have an impact on the vascular system, such as diabetes, peripheral arterial disease, and chronic edema, can interfere with reliability. In addition, we suggest that future studies of reliability consider other peripheral arteries and veins.
AND
CONFLICTS
OF INTEREST
CONTRIBUTORSHIP INFORMATION Concept development (provided idea for the research): E.C.O.G., R.R.J.G., A.V.D.F. Design (planned the methods to generate the results): E.C.O.G., R.R.J.G., A.V.D.F. Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): E.C.O.G., R.R.J.G. Data collection/processing (responsible for experiments, patient management, organization, or reporting data): N.C.S.B., G.P.M.F.L. Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): A.V.D.F. Literature search (performed the literature search): N.C.S.B., G.P.M.F.L., A.V.D.F. Writing (responsible for writing a substantive part of the manuscript): N.C.S.B., G.P.M.F.L., A.V.D.F., E.C.O.G., R.R.J.G. Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): E.C.O.G., R.R.J.G., A.V.D.F.
Practical Applications
• The measurement of mean and maximum blood flow velocity by means of the Doppler ultrasound can be used in clinical practice to assess the brachial, radial, popliteal, and posterior tibial arteries.
REFERENCES 1. Young M, Birch I, Potter CA, et al. A comparison of the Doppler ultrasound interpretation by student and registered podiatrists. J Foot Ankle Res. 2013;6:25.
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2. Matheus CN, Guirro EC. Change in blood flow velocity demonstrated by Doppler ultrasound in upper limb after axillary dissection surgery for the treatment of breast cancer. Breast Cancer Res Treat. 2011;127(3):697-704. 3. Singh N, Armstrong DG, Lipsky B. Preventing foot ulcers in patients with diabetes. JAMA. 2005;293(2):217-228. 4. Svensson WE, Mortimer PS, Tohno E, Cosgrove DO. Increased arterial inflow demonstrated by Doppler ultrasound in arm swelling following breast cancer treatment. Eur J Cancer. 1994; 30A(5):661-664. 5. Moraska AF, Hickner RC, Kohrt WM, Brewer A. Changes in blood flow and cellular metabolism at a myofascial trigger point with trigger point release (ischemic compression): a proof-of-principle pilot study. Arch Phys Med Rehabil. 2013; 94(1):196-200. 6. Guirro EC, Guirro RR, Dibai-Filho AV, Pascote SC, Rodrigues-Bigaton D. Immediate effects of electrical stimulation, diathermy, and physical exercise on lower limb arterial blood flow in diabetic women with peripheral arterial disease: a randomized crossover trial. J Manip Physiol Ther. 2015; 38(3):195-202. 7. Yao JS. Noninvasive studies of peripheral vascular disease. In: Hobson RW, Wilson SE, Veith FJ, editors. Vascular Surgery: Principles and Practice. 3rd ed. New York, NY: Marcell Deckker; 2004. p. 113-122. 8. Sabbà C, Merkel C, Zoli M, et al. Interobserver and interequipment variability of echo-Doppler examination of the portal vein: effect of a cooperative training program. Hepatology. 1995; 21(2):428-433. 9. Sacerdoti D, Gaiani S, Buonamico P, et al. Interobserver and interequipment variability of hepatic, splenic, and renal arterial Doppler resistance indices in normal subjects and patients with cirrhosis. J Hepatol. 1997;27(6):986-992. 10. Berzigotti A, Reverter E, García-Criado A, et al. Reliability of the estimation of total hepatic blood flow by Doppler ultrasound in patients with cirrhotic portal hypertension. J Hepatol. 2013; 59(4):717-722. 11. de Oliveira CA, de Sá RA, Velarde LG, Monteiro VN, Netto HC. Doppler velocimetry of the ophthalmic artery: reproducibility of blood flow velocity measurements. J Ultrasound Med. 2012; 31(6):879-884. 12. Ventura W, De Paco C, Delgado JL, Blanco JE, Peñalver C, Parrilla JJ. Reliability of examining the external iliac artery with Doppler ultrasound in the first trimester and its relationship with maternal blood pressure and uterine artery blood flow. Eur J Obstet Gynecol Reprod Biol. 2012;165(1): 42-46. 13. Vingerhoets G, Stroobant N. Reliability and validity of day-today blood flow velocity reactivity in a single subject: an fTCD study. Ultrasound Med Biol. 2002;28(2):197-202. 14. Shoemaker JK, Pozeg ZI, Hughson RL. Forearm blood flow by Doppler ultrasound during test and exercise: tests of day-to-day repeatability. Med Sci Sports Exerc. 1996;28(9):1144-1149. 15. Walther G, Nottin S, Dauzat M, Obert P. Femoral and axillary ultrasound blood flow during exercise: a methodological study. Med Sci Sports Exerc. 2006;38(7):1353-1361. 16. Labropoulos N, Watson WC, Mansour MA, Kang SS, Littooy FN, Baker WH. Acute effects of intermittent pneumatic compression on popliteal artery blood flow. Arch Surg. 1998; 133(10):1072-1075.
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17. Terwee CB, Bot SD, de Boer MR, et al. Quality criteria were proposed for measurement properties of health status questionnaires. J Clin Epidemiol. 2007;60(1):34-42. 18. Altman DG. Practical Statistics for Medical Research. London: Chapman and Halled; 1991. 19. Costa AC, Dibai Filho AV, Packer AC, Rodrigues-Bigaton D. Intra- and inter-rater reliability of infrared image analysis of masticatory and upper trapezius muscles in women with and without temporomandibular disorder. Braz J Phys Ther. 2013; 17(1):24-31. 20. Tucci HT, Martins J, Sposito Gde C, Camarini PM, de Oliveira AS. Closed Kinetic Chain Upper Extremity Stability test (CKCUES test): a reliability study in persons with and without shoulder impingement syndrome. BMC Musculoskelet Disord. 2014;15:1. 21. Weir JP. Quantifying test-retest reliability using the intraclass correlation coefficient and the SEM. J Strength Cond Res. 2005;19(1):231-240. 22. Dibai-Filho AV, Guirro EC, Ferreira VT, Brandino HE, Vaz MM, Guirro RR. Reliability of different methodologies of infrared image analysis of myofascial trigger points in the upper trapezius muscle. Braz J Phys Ther. 2015;19(1):122-128. 23. Martinho NM, Marques J, Silva VR, Silva SL, Carvalho LC, Botelho S. Intra and inter-rater reliability study of pelvic floor muscle dynamometric measurements. Braz J Phys Ther. 2015; 19(2):97-104. 24. Mutchler JA, Weinhandl JT, Hoch MC, Van Lunen BL. Reliability and fatigue characteristics of a standing hip isometric endurance protocol. J Electromyogr Kinesiol. 2015;25(4): 667-674. 25. Kottner J, Audigé L, Brorson S, et al. Guidelines for Reporting Reliability and Agreement Studies (GRRAS) were proposed. J Clin Epidemiol. 2011;64(1):96-106. 26. Guirro EC, Guirro RR, Dibai-Filho AV, Montezuma T, Vaz MM. Decrease in talocrural joint mobility is related to alteration of the arterial blood flow velocity in the lower limb in diabetic women. J Phys Ther Sci. 2014;26(4):553-556. 27. Osada T. Physiological aspects of the determination of comprehensive arterial inflows in the lower abdomen assessed by Doppler ultrasound. Cardiovasc Ultrasound. 2012;10:13. 28. Billinger SA, Kluding PM. Use of Doppler ultrasound to assess femoral artery adaptations in the hemiparetic limb in people with stroke. Cerebrovasc Dis. 2009;27(6):552-558. 29. McDonnell MN, Berry NM, Cutting MA, Keage HA, Buckley JD, Howe PR. Transcranial Doppler ultrasound to assess cerebrovascular reactivity: reliability, reproducibility and effect of posture. PeerJ. 2013;1e65. 30. Crisóstomo RS, Candeias MS, Armada-da-Siva PA. The use of ultrasound in the evaluation of the efficacy of calf muscle pump function in primary chronic venous disease. Phlebology. 2014; 29(4):247-256. 31. Fernandez S, Figueras F, Gomez O, et al. Intra- and interobserver reliability of umbilical vein blood flow. Prenat Diagn. 2008; 28(11):999-1003. 32. Lin Q, Dai Z, Xia M, et al. A connectivity-based test-retest dataset of multi-modal magnetic resonance imaging in young healthy adults. Sci Data. 2015;2:150056. 33. Mitchell D, Hancock E, Alexander L. An investigation of the inter-rater reliability of the Valpar Joule functional capacity evaluation in healthy adults. Work. 2015;53(2):337-345.
INTRODUCTION The evaluation of peripheral blood flow is extremely important in clinical practice for the diagnosis of circulatory system changes. 1 The decrease in the blood flow velocity indicates a reduction in the caliber of the vessels, which may suggest the occurrence of stenosis or vascular lumen obstruction. 2 In this sense, determining the blood flow velocity of peripheral arteries is a procedure that has been employed with various purposes, such as the detection of peripheral artery Postgraduate Program in Rehabilitation and Functional Performance, Department of Biomechanics, Medicine, and Rehabilitation of the Locomotor Apparatus, Medical School of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil. Corresponding author: Elaine Caldeira de Oliveira Guirro, PT, PhD, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Curso de Fisioterapia, Avenida dos Bandeirantes, 3900, Monte Alegre, Ribeirão Preto, SP, Brasil, CEP 14049-900. (e-mail: [email protected]). Paper submitted August 25, 2015; in revised form November 18, 2015; accepted April 5, 2016. 0161-4754 Copyright © 2017 by National University of Health Sciences. http://dx.doi.org/10.1016/j.jmpt.2017.02.007
diseases; classification of the risk of a patient developing ulcers, gangrene, and amputation 3; diagnosis of circulatory dysfunctions after surgeries 2,4; and assessment of effects of the therapeutic resources on blood circulation. 5,6 Doppler ultrasound is a noninvasive method for the evaluation of blood circulation. The transducer is placed on the site to be evaluated using gel as a conductor, with an approximate angle of 30°, and the ultrasonic waves are emitted and projected obliquely to the blood flow, being reflected by erythrocytes and producing spectral analysis and calculation of the hematological profile found. 7 Although Doppler ultrasound is widely used for this purpose, it is known that absolute measurements of arterial blood flow depend on several factors, such as the examiner, patient, equipment, protocols, and environment of application. 4,8,9 Even considering a possible variability of results, few studies have focused on reliability and reproducibility of the blood flow velocity variable identified by the Doppler ultrasound device. However, studies on hepatic, 10 ophthalmic, 11 uterine, 12 and brain 13 arteries reveal that, with standardization of evaluations, Doppler ultrasound has good reliability of results, both in terms of the time and examiners. Based on these considerations, and although studies have investigated the behavior of the blood flow in different
Journal of Manipulative and Physiological Therapeutics Volume 40, Number 4
arteries, such as the brachial, 14 femoral, 15 and popliteal, 16 the reliability of Doppler ultrasound on peripheral arteries has not yet been completely established. Thus, the present study aimed to evaluate the intra- and inter-rater reliability of the measurement of the blood flow velocity by means of Doppler ultrasound in the brachial, radial, popliteal, and posterior tibial arteries. The hypothesis of this study was that the evaluation of blood flow velocity has acceptable reliability values for its use in research and in clinical settings.
METHODS Sample The sample size was based on the guidelines for the evaluation of measurement properties, 17 in which at least 50 participants would be necessary to evaluate the reproducibility and validity of the construct. 18 Thus, 51 volunteers were recruited by means of verbal invitation and posters in the university community of Ribeirão Preto (SP, Brazil). In this study, we included volunteers without health issues that could compromise analyses (healthy individuals) of both genders and aged between 18 and 45 years. As exclusion criteria, we adopted the presence of circulatory or metabolic diseases, systemic diseases that affect the circulatory system, neurologic or neuromuscular diseases, use of drugs that affect the circulatory system, and treatment with physical therapy or physical activity during the data collection period. In the face of these eligibility criteria, there was sample loss of 1 volunteer as a result of nonattendance in the second session, and thus the final sample was composed of 50 individuals. This study was approved by the Research Ethics Committee of Clinics Hospital of the Medical School of Ribeirão Preto of the University of São Paulo under protocol number 313882/2013.
Doppler Ultrasound For the evaluation of arterial blood flow velocity, a portable Doppler device SONAR/tek (Nicolet Vascular, Natus, San Carlos, CA) was used with spectral analysis and data about components of the flow profile. The volunteers were examined after 10 minutes of rest in the dorsal decubitus position in an air-conditioned room at 23°C and humidity of 50%. The evaluations were performed in dominant lower and upper limbs. Two examiners captured Doppler signals from posterior tibial and radial arteries with a probe of 8 MHz and from popliteal and brachial arteries with a probe of 4 MHz, which were used as a parameter the mean and maximum velocity of the arterial blood flow (in cm/s). Three collections for each artery (each windowing with 10 seconds) were carried out, considering the mean for statistical calculations. The order to measure the arteries was randomized.
Guirro et al Reliability of Doppler Ultrasound
Evaluation Procedure Signal processing was performed with SONARA/tek software, considering the entire period of collection. The evaluations of velocity in arteries were conducted by 2 examiners previously trained in use of the Doppler ultrasound. The examiners performed evaluations with the same volunteers independently and twice, with an interval of 1 week between them, 19 thus enabling the measurement of intra- and inter-rater reliability.
Statistical Analysis The intraclass correlation coefficient (ICC3,2) was used to determine the intra- and inter-rater reliability, with their respective 95% confidence intervals, standard errors of measurement (SEM), and minimum detectable change (MDC), according to Tucci et al. 20 The interpretation of ICC values was based on that suggested by Weir. 21 For values ranging from 1.00 to 0.81, the reliability was considered excellent; from 0.80 to 0.61, very good; from 0.60 to 0.41, good; from 0.40 to 0.21, reasonable; and finally, from 0.20 to 0.00, poor. All the statistical analysis was performed using the Statistical Package for Social Sciences software, version 17.0 (SPSS Inc., Chicago, IL).
RESULTS The sample of the present study was composed of 50 individuals of both genders (40 women, 10 men) and 43 righthanders, with mean age of 25.10 years (standard deviation [SD] = 4.18) and mean body mass index of 22.89 kg/m 2 (SD = 3.72). The values of mean and maximum velocity of arterial blood flow obtained by both examiners are described in Table 1. Table 2 presents the values of intrarater reliability from the measurement of mean velocity of arterial blood flow, and good to very good reliability was noted, with ICC values ranging between 0.510 and 0.722, SEM values ranging between 1.17 and 2.67 cm/s, and MDC values ranging between 3.25 and 7.37 cm/s. With regard to the inter-rater reliability from the measurement of mean velocity of arterial blood (Table 3), very good reliability was noted, with ICC values ranging between 0.700 and 0.780, SEM values ranging between 0.81 and 2.10 cm/s, and MDC values ranging between 2.55 and 5.82 cm/s. The values of intrarater reliability from the measurement of maximum velocity of arterial blood flow are in Table 4. Good to very good reliability was noted, with ICC values ranging between 0.539 and 0.659, SEM values ranging between 3.80 and 9.41 cm/s, and MDC values ranging between 10.50 and 26.13 cm/s. With regard to the inter-rater reliability from the measurement of maximum velocity of arterial blood (Table 5), good to very good reliability was noted, with ICC values ranging between 0.595 and 0.866, SEM values ranging
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Table 1. Description of Values of Mean and Maximum Velocity of Arterial Blood Flow (in cm/s) Obtained by Both Examiners Blood Flow
Artery
Examiner 1
Examiner 2
Test
Retest
Test
Retest
Brachial
Mean Maximum
13.28 (3.99) 59.03 (10.54)
12.92 (3.16) 57.07 (9.55)
11.49 (3.78) 52.28 (11.51)
12.41 (4.52) 54.53 (14.27)
Radial
Mean Maximum
4.09 (1.86) 23.88 (6.06)
3.99 (1.21) 24.67 (5.31)
4.36 (2.14) 25.70 (6.96)
4.38 (1.62) 26.57 (7.71)
Popliteal
Mean Maximum
8.52 (3.59) 38.90 (16.28)
8.46 (3.40) 38.11 (14.99)
7.72 (3.41) 35.20 (12.49)
7.99 (3.99) 34.45 (14.69)
Posterior tibial
Mean Maximum
4.86 (2.14) 27.00 (9.20)
4.63 (1.82) 26.76 (8.08)
5.45 (3.43) 28.23 (10.17)
5.06 (2.17) 28.95 (7.97)
Values shown as mean (standard deviation).
Table 2. Intrarater Reliability of the Measurement of Mean Blood Flow Velocity of Peripheral Arteries With Doppler Ultrasound
Table 3. Inter-rater Reliability of the Measurement of Mean Blood Flow Velocity of Peripheral Arteries With Doppler Ultrasound
Artery
ICC
95% CI
SEM
MDC
Artery
ICC
95% CI
SEM
MDC
Brachial Radial Popliteal Posterior tibial
0.519 0.520 0.501 0.722
0.153, 0.727 0.153, 0.727 0.120, 0.717 0.510, 0.842
2.67 1.17 2.53 1.63
7.37 3.25 7.00 4.53
Brachial Radial Popliteal Posterior tibial
0.702 0.769 0.780 0.700
0.474, 0.831 0.592, 0.869 0.613, 0.875 0.472, 0.830
2.10 0.81 1.68 1.70
5.82 2.25 4.65 4.70
CI, confidence interval; ICC, intraclass correlation coefficient; MDC, minimum detectable change (in cm/s); SEM, standard error of measurement (in cm/s).
CI, confidence interval; ICC, intraclass correlation coefficient; MDC, minimum detectable change (in cm/s); SEM, standard error of measurement (in cm/s).
between 2.98 and 8.14 cm/s, and MDC values ranging between 8.25 and 22.51 cm/s.
peripheral arteries, including the establishment of the standard error of measurement and minimum detectable change. Thus, our study presents this uniqueness and identified ICC values lower than Guirro et al. 6 However, according to the reference established by Weir, 21 good to very good reliability was identified in the present study, with intrarater ICC raging between 0.501 and 0.722 and inter-rater ranging between 0.595 and 0.866. In this context, Osada 27 reported intrarater ICC values of 0.94, 0.90, and 0.85 for the blood flow of the abdominal aortic, left femoral, and right femoral arteries, respectively. Billinger and Kluding 28 reported intra-rater ICC values of 0.96 and 0.98 for the measurement of femoral blood flow velocity of the hemiparetic and nonhemiparetic limbs, respectively, in people with stroke. In their turn, McDonnell et al 29 evaluated the blood flow velocity of intracranial arteries in different positions and obtained intrarater ICC values of 0.822 for the seated volunteers and 0.734 for the lying volunteers and inter-rater ICC values of 0.504 for sitting and 0.081 for the lying position. However, comparisons between our study and the previously mentioned investigations must be made with caution, given that anatomic location influences reliability, although all of them recommend Doppler ultrasound for the evaluation of arterial blood flow. Other authors have evaluated the reliability of measuring the blood flow velocity of veins. Crisóstomo et al 30 evaluated the intrarater reliability of peak blood flow velocity of the popliteal vein in patients with primary chronic venous disease by means of Doppler ultrasound at baseline and during 3 sets of 10 tiptoe movement repetitions and noted that the reliability
DISCUSSION Good to very good reliability for the measurement of mean and maximum velocity of blood flow in the posterior tibial, popliteal, brachial, and radial arteries by means of Doppler ultrasound was identified in the present study. It is worth noting the recent focus of several studies on this property of instruments of biological signals assessment. 22-24 Complementing and highlighting the importance of investigations on the topic of this study, Kottner et al 25 observed that results of reliability and agreement studies provide information about the amount of error inherent in any diagnosis, score, or measurement, where the amount of measurement error determines the validity of the study results or scores. Although previous studies have investigated the behavior of blood flow velocity of peripheral arteries in diverse populations, 2,15,26 the scientific literature provides scarce information on the reliability of Doppler ultrasound in these arteries. Only the crossover clinical trial conducted by Guirro et al. 6 performed the analysis of intrarater reliability of the maximum blood flow velocity as a complement to the data analysis and found an ICC value of 0.796 for popliteal artery and ICC value of 0.899 for posterior tibial artery. The study in question did not evaluate arteries of the upper limb. Moreover, the authors suggested that future studies should be developed focusing on the intra- and inter-rater reliability in various
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Guirro et al Reliability of Doppler Ultrasound
Table 4. Intrarater Reliability of the Measurement of Maximum Blood Flow Velocity of Peripheral Arteries With Doppler Ultrasound Artery
ICC
95% CI
SEM
MDC
Brachial Radial Popliteal Posterior tibial
0.539 0.659 0.581 0.602
0.187, 0.738 0.399, 0.806 0.262, 0.762 0.299, 0.774
7.78 3.80 9.45 5.58
21.50 10.50 26.13 15.42
CONCLUSION The assessment of mean and maximum blood flow velocity of brachial, radial, popliteal, and posterior tibial arteries by means of Doppler ultrasound presents acceptable reliability values, which supports the use of this evaluation method in research and clinical practice.
CI, confidence interval; ICC, intraclass correlation coefficient; MDC, minimum detectable change (in cm/s); SEM, standard error of measurement (in cm/s).
FUNDING SOURCES
Table 5. Inter-rater Reliability of the Measurement of Maximum
No funding sources or conflicts of interest were reported for this study.
Blood Flow Velocity of Peripheral Arteries With Doppler Ultrasound Artery
ICC
95% CI
SEM
MDC
Brachial Radial Popliteal Posterior tibial
0.595 0.702 0.689 0.866
0.287, 0.770 0.476, 0.831 0.451, 0.823 0.764, 0.924
7.29 3.55 8.14 2.98
20.15 9.82 22.51 8.25
CI, confidence interval; ICC, intraclass correlation coefficient; MDC, minimum detectable change (in cm/s); SEM, standard error of measurement (in cm/s).
of peak blood flow velocity was high (ICC = 0.70) for values obtained in the first contraction of the set but lowered when using the last contraction (ICC b 0.50). In addition to this study, Fernandez et al 31 found values of intra- and inter-rater ICC of 0.59 and 0.46, respectively, when measuring the maximum blood flow velocity of the umbilical vein. In these terms, although the arterial and venous blood flows have distinct features, such as vessel structure, anatomic location, and flow type, the results of these investigations are similar to that of our study, in which most of ICC values were between 0.501 and 0.780. The description of SEM and MDC values was not found in studies of the literature that focused on the reliability of measurement of blood flow velocity by Doppler ultrasound. In current times, these 2 indicators are necessary for studies that evaluate reliability. SEM indicates errors during the measurement of a particular variable with an evaluative tool; in other words, it is an indication of the precision of a score. 21 With regards to MDC, Tucci et al 20 highlighted that it is important to have knowledge about the minimal difference in the scores of an evaluation tool between revaluation sessions that could be considered a real improvement with no error. Therefore, we suggest that future studies should implement the calculation of SEM and MDC in their statistical analysis to establish error parameters in measurements. The calculation of the Doppler ultrasound reliability was conducted in healthy participants, which is common in other published investigations. 19,32,33 However, we emphasize that the presence of diseases that have an impact on the vascular system, such as diabetes, peripheral arterial disease, and chronic edema, can interfere with reliability. In addition, we suggest that future studies of reliability consider other peripheral arteries and veins.
AND
CONFLICTS
OF INTEREST
CONTRIBUTORSHIP INFORMATION Concept development (provided idea for the research): E.C.O.G., R.R.J.G., A.V.D.F. Design (planned the methods to generate the results): E.C.O.G., R.R.J.G., A.V.D.F. Supervision (provided oversight, responsible for organization and implementation, writing of the manuscript): E.C.O.G., R.R.J.G. Data collection/processing (responsible for experiments, patient management, organization, or reporting data): N.C.S.B., G.P.M.F.L. Analysis/interpretation (responsible for statistical analysis, evaluation, and presentation of the results): A.V.D.F. Literature search (performed the literature search): N.C.S.B., G.P.M.F.L., A.V.D.F. Writing (responsible for writing a substantive part of the manuscript): N.C.S.B., G.P.M.F.L., A.V.D.F., E.C.O.G., R.R.J.G. Critical review (revised manuscript for intellectual content, this does not relate to spelling and grammar checking): E.C.O.G., R.R.J.G., A.V.D.F.
Practical Applications
• The measurement of mean and maximum blood flow velocity by means of the Doppler ultrasound can be used in clinical practice to assess the brachial, radial, popliteal, and posterior tibial arteries.
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