Valores de referência ultrassonográficos para áreas e índices de secção transversa de nervos periféricos em uma amostra de indivíduos brasileiros saudáveis

Voltan, Glauber; Bernardes-Filho, Fred; Lugão, Helena Barbosa; Nogueira-Barbosa, Marcello Henrique; Frade, Marco Andrey Cipriani

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Original Article • Radiol Bras 55 (6) • Nov-Dec 2022 • https://doi.org/10.1590/0100-3984.2022.0020 copiar

Valores de referência ultrassonográficos para áreas e índices de secção transversa de nervos periféricos em uma amostra de indivíduos brasileiros saudáveis

Autoria SCIMAGO INSTITUTIONS RANKINGS

Resumo

Objetivo:

Estabelecer valores de referência da área de secção transversa (AST) dos nervos periféricos (valores absolutos e medidas de assimetria e de espessamento focal) para amostra de indivíduos brasileiros saudáveis.

Materiais e Métodos:

Sessenta e seis voluntários brasileiros saudáveis foram submetidos a ultrassonografia de alta resolução de nervos periféricos. As medidas da AST dos seguintes nervos periféricos foram obtidas em: mediano no túnel do carpo (MT), ulnar no túnel cubital (UT), pré-túnel ulnar (UPT) e fibular comum na cabeça da fíbula (FH). Os índices CSA foram obtidos entre os mesmos sítios em lados diferentes (∆CSA) e entre os sítios distal e proximal do nervo ulnar (∆TPT).

Resultados:

As seguintes médias ± desvio-padrão e mediana da AST foram obtidas para os 132 sítios dos nervos periféricos analisados: MT (6,3 ± 1,9 mm²; 6,0 mm²), UT (6,2 ± 1,6 mm²; 6,1 mm²), UPT (5,6 ± 1,7 mm²; 5,4 mm²) e FH (10,0 ± 3,7 mm²; 9,9 mm²). A média ± desvio-padrão e as respectivas medianas do ∆CSA em mm² foram: 0,85 ± 0,7 [0,95] para MT, 0,81 ± 0,62 [0,95] para UT, 0,61 ± 0,51 [0,5] para UPT, 1,0 ± 0,77 [1] para FH, e 1,0 ± 0,8 [1,0] para ∆TPT.

Conclusão:

Os valores de AST tendem a ser maiores no sexo masculino, aumentando os valores absolutos das medianas das ASTs com o envelhecimento, mas não nos seus índices, ∆CSA e ∆TPT, exceto a diferença entre a AST dos nervos ulnares nos lados direito e esquerdo. Diferenças de valores de AST entre lados ou pontos no mesmo nervo maior que 2,5 mm² podem significar neuropatia com assimetria e espessamento focal.

Unitermos:
Nervos periféricos/diagnóstico por imagem; Ultrassonografia; Valores de referência.

Variable	Approach	Equation
Asymmetry	Ratio	= [maximum CSA (right/left)] - [minimum CSA (right/left)]
Asymmetry	Difference	∆MT = [maximum CSA MT (right/left)] - [minimum CSA MT (right/left)] ∆UT = [maximum CSA UT (right/left)] - [minimum CSA UT (right/left)] ∆UΡT = [maximum CSA UPT (right/left)] - [minimum CSA UPT (right/left)] ∆FH = [maximum CSA FH (right/left)] - [minimum CSA FH (right/left)]
Focality	Ratio	= [maximum CSA (UT/UPT)] - [minimum CSA (UT/UPT)]
Focality	Difference	∆TΡT = [maximum CSA (UT/UPT)] - [minimum CSA (UT/UPT)]

	Age range (years)					Upper limit (mean + 2 SD)
Variables	7-14	15-30	31-45	46-60	15-60	Upper limit (mean + 2 SD)
Sex
Male, n	6	12	4	6	22
Female, n	11	12	11	4	27
Total (R + L), n	34	48	30	20	98
Overall CSA, mean ± SD [median] CSA (mm²), mean ± SD [median]	11.7 ± 2.1 [12.0]	22.9 ± 4.6 [23.0]	37.0 ± 4.6 [36.0]	49.6 ± 2.5 [49.0]	27 ± 13 [25.0]
MT	5.5 ± 1.7 [5.0]	6.7 ± 2.0 [6.0]	6.8 ± 2.0 [6.2]	6.4 ± 1.2 [6.3]	6.6 ± 1.9 [6.0]	10.4
UT	5.2 ± 1.4 [6.0]	6.6 ± 1.7 [6.2]	6.6 ± 1.5 [6.7]	6.7 ± 1.0 [7.0]	6.7 ± 1.5 [6.1]	9.7
UPT	4.6 ± 1.2 [5.0]	6.3 ± 2.1 [5.8]	5.7±1.3 [5.6]	6.0±1.2 [6.3]	6.0 ± 1.7 [5.4]	9.4
FH	8.5 ± 3.0 [8.6]	10.7 ± 3.4 [11.0]	10.6 ± 4.8 [10.5]	10.9±2.9[10]	10.7 ± 3.8 [9.9]	18.3
∆CSA (mm²), mean ± SD [median]
MT	0.84 ± 0.6 [0.9]	0.6 ± 0.7 [0.4]	1.0 ± 0.7 [1.0]	0.9±0.8 [0.8]	0.8 ± 0.7 [0.9]	2.2
UT	0.6 ± 0.5 [1.0]	1.0 ± 0.7 [1.0]	0.8 ± 0.5 [0.9]	0.8±0.6 [0.7]	0.9 ± 0.6 [0.9]	3.1
UPT	0.6 ± 0.6 [0.3]	0.7 ± 0.4 [0.5]	0.6 ± 0.6 [0.4]	0.8±0.6 [0.5]	0.6 ± 0.4 [0.5]	1.4
FH	1.2 ± 0.9 [1.0]	0.9 ± 0.7 [0.75]	0.9 ± 0.6 [0.8]	1.1±0.8 [1.0]	0.9 ± 0.7 [1.0]	2.3
∆TPT (mm²), mean ± SD [median]	1.0 ±0.8 [1.0]	0.9 ± 0.8 [0.65]	1.2 ± 0.8 [1.1]	0.7±0.6 [0.6]	1.0 ± 0.8 [1.0]	2.6
CSA ratio, mean ± SD [median]
MT	1.2 ± 0.3 [1.2]	1.1 ± 0.1 [1.1]	1.2 ± 0.1 [1.1]	1.2±0.1 [1.1]	1.1 ± 0.14 [1.1]	1.38
UT	1.1 ± 0.1 [1.0]	1.2 ± 0.2 [1.2]	1.1 ± 0.1 [1.1]	1.1±0.1 [1.1]	1.1 ± 0.12 [1.1]	1.34
UPT	1.2 ± 0.2 [1.0]	1.1 ± 0.1 [1.1]	1.1 ± 0.1 [1.1]	1.0±0.0 [1.0]	1.13 ± 0.14 [1]	1.41
FH	1.2 ± 0.1 [1.1]	1.1 ± 0.1 [1.1]	1.1 ± 0.1 [1.1]	1.1±0.1 [1.0]	1.1 ± 0.10 [1.1]	1.3
TPT ratio, mean ± SD [median]	1.2 ± 0.2 [1.2]	1.2 ± 0.2 [1.1]	1.2 ± 0.2 [1.2]	1.1±0.2 [1.0]	1.2 ± 0.19 [1.2]	1.58

	Current study		Frade et al.(¹⁶16 Frade MAC, Nogueira-Barbosa MH, Lugão HB, et al. New sonographic measures of peripheral nerves: a tool for diagnosis of peripheric nerve involvment in leprosy. Mem Inst Oswaldo Cruz. 2013;108:257-62.)	Kerasnoudis et al.(¹³13 Kerasnoudis A, Pitarokoili K, Behrendt V, et al. Cross sectional area reference values for sonography of peripheral nerves and brachial plexus. Clin Neurophysiol. 2013;124:1881-8.)	Won et al.(¹⁸18 Won SJ, Kim BJ, Park KS, et al. Reference values for nerve ultrasonography in the upper extremity. Muscle Nerve. 2013;47:864-71.)	Qrimli et al.(²2 Qrimli M, Ebadi H, Breiner A, et al. Reference values for ultrasonography of peripheral nerves. Muscle Nerve. 2016;53:538-44.)
Parameter	Difference (∆)	Ratio	Difference (∆)	Ratio	Ratio	Difference, ∆
Equation	Maximum (R or L) - minimum (R or L)	Maximum (R or L) ∕ minimum (R or L)	Maximum (R or L) - minimum (R or L)	Side-to-side R/L	R - L ∕ (< R or L) × 100	Upper limit side-to-side
N	66	66	46 or 48^* * 46 for the UT and UPT; 48 for the MT and FH.	75	97	100
Age range (years)	15-60	15-60	≥ 18	≥ 18	20-69	≥ 18
CSA, mean ± SD
MT	0.85 ± 0.7	1.1 ± 0.14	1.0 ± 0.8	1.21 ± 0.04	-	3.3
UT	0.81 ± 0.62	1.1 ± 0.12	1.0 ± 0.7	1.2 ± 0.25	1.31 ± 0.25	2.5
UPT	0.61 ± 0.51	1.13 ± 0.14	0.9 ± 0.7	-	1.25 ± 0.2	2.5
FH	1.0 ± 0.77	1.1 ± 0.10	1.1 ± 1.1	1.19 ± 0.23	-	4.3
Ulnar TPT, mean ± SD	1.0 ± 0.81	1.2 ± 0.19	1.4 ± 1.1	1.5 ± 0.5	-	-

	Neural site
	MT				UT				UPT				FH
Reference	Nerves (n)	Mean	SD	P ^* * Results of the present study versus those of the studies included in the systematic review.	Nerves (n)	Mean	SD	P ^* * Results of the present study versus those of the studies included in the systematic review.	Nerves (n)	Mean	SD	P ^* * Results of the present study versus those of the studies included in the systematic review.	Nerves (n)	Mean	SD	P ^* * Results of the present study versus those of the studies included in the systematic review.
Lothet et al.(²⁹29 Lothet EH, Bishop TJ, Walker FO, et al. Ultrasound-derived nerve cross-sectional area in extremes of height and weight. J Neuroimaging. 2019;29:406-9.)	50	10	2.6	< 0.001	30	8.2	1.3	0.8	-	-	-	-	60	11.2	3.3	0.03
Bedewi et al.(²⁷27 Bedewi MA, Abodonya A, Kotb M, et al. Estimation of ultrasound reference values for the lower limb peripheral nerves in adults: a cross-sectional study. Medicine (Baltimore). 2018;97:e0179.)	138	9.8	2.8	< 0.001	138	7.5	2.3	< 0.001	138	7.6	2.6	< 0.001	138	8.9	3.2	0.006
Druzhinin et al.(²⁶26 Druzhinin D, Naumova E, Nikitin S. Nerve ultrasound normal values in children and young adults. Muscle Nerve. 2019;60:757-61.)	44^† † The authors considered only individuals ≥ 15 years of age (n = 22).	6.58	1.97	0.403	44^† † The authors considered only individuals ≥ 15 years of age (n = 22).	5.78	1.9	0.153	44^† † The authors considered only individuals ≥ 15 years of age (n = 22).	6.41	2.1	0.011	44^† † The authors considered only individuals ≥ 15 years of age (n = 22).	7.82	2.2	< 0.001
Kerasnoudis et al.(¹³13 Kerasnoudis A, Pitarokoili K, Behrendt V, et al. Cross sectional area reference values for sonography of peripheral nerves and brachial plexus. Clin Neurophysiol. 2013;124:1881-8.)	150	8	2	< 0.001	-	-	-	-	-	-	-	-	-	-	-	-
Cartwright et al.(²¹21 Cartwright MS, Shin HW, Passmore LV, et al. Ultrasonographic reference values for assessing the normal median nerve in adults. J Neuroimaging. 2009;19:47-51.)	100	9.8	2.4	< 0.001	-	-	-	-	-	-	-	-	-	-	-	-
Boehm et al.(¹⁰10 Boehm J, Scheidl E, Bereczki D, et al. High-resolution ultrasonography of peripheral nerves: measurements on 14 nerve segments in 56 healthy subjects and reliability assessments. Ultraschall Med. 2014; 35:459-67.)	56	8.5	1.8	< 0.001	56	7.6	2.1	< 0.001	56	6.3	1.6	0.009	56	8.9	2	0.037
Grimm et al.(²⁴24 Grimm A, Axer H, Heiling B, et al. Nerve ultrasound normal values - readjustment of the ultrasound pattern sum score UPSS. Clin Neurophysiol. 2018;129:1403-9.)	100^‡ ‡ The authors considered only the right side for neural site measurements; therefore, the number of individuals was equal to the number of nerves evaluated.	10.6	2.9	< 0.001	100^‡ ‡ The authors considered only the right side for neural site measurements; therefore, the number of individuals was equal to the number of nerves evaluated.	8.7	2.9	< 0.001	100^‡ ‡ The authors considered only the right side for neural site measurements; therefore, the number of individuals was equal to the number of nerves evaluated.	7	1.2	< 0.001	100^‡ ‡ The authors considered only the right side for neural site measurements; therefore, the number of individuals was equal to the number of nerves evaluated.	8.4	1.6	< 0.001
Frade et al.(¹⁶16 Frade MAC, Nogueira-Barbosa MH, Lugão HB, et al. New sonographic measures of peripheral nerves: a tool for diagnosis of peripheric nerve involvment in leprosy. Mem Inst Oswaldo Cruz. 2013;108:257-62.)	96	5.9	1.5	0.09	92	6.7	2.2	0.05	92	5.9	1.8	0.21	96	8.2	4.4	0.001
Qrimli et al.(²2 Qrimli M, Ebadi H, Breiner A, et al. Reference values for ultrasonography of peripheral nerves. Muscle Nerve. 2016;53:538-44.)	100^‡ ‡ The authors considered only the right side for neural site measurements; therefore, the number of individuals was equal to the number of nerves evaluated.	10.2	2.4	< 0.001	100^‡ ‡ The authors considered only the right side for neural site measurements; therefore, the number of individuals was equal to the number of nerves evaluated.	6.9	2.3	0.007	100^‡ ‡ The authors considered only the right side for neural site measurements; therefore, the number of individuals was equal to the number of nerves evaluated.	6.8	2.3	< 0.001	100^‡ ‡ The authors considered only the right side for neural site measurements; therefore, the number of individuals was equal to the number of nerves evaluated.	11.1	3.5	0.023
Won et al.(¹⁸18 Won SJ, Kim BJ, Park KS, et al. Reference values for nerve ultrasonography in the upper extremity. Muscle Nerve. 2013;47:864-71.)	194	8.3	1.5	< 0.001	-	-	-	-	194	5.8	1	0.18	-	-	-	-
Cartwright et al.(²⁰20 Cartwright MS, Passmore LV, Yoon JS, et al. Cross-sectional area reference values for nerve ultrasonography. Muscle Nerve. 2008;37: 566-71.)	-	--	-	-	-	-	-	-	-	-	-	-	120	11.2	3.3	0.007
Seok et al.(²³23 Seok HY, Jang JH, Won SJ, et al. Cross-sectional area reference values of nerves in the lower extremities using ultrasonography. Muscle Nerve. 2014;50:564-70.)	-	-	-	-	-	-	-	-	-	-	-	-	94^‡ ‡ The authors considered only the right side for neural site measurements; therefore, the number of individuals was equal to the number of nerves evaluated.	9.2	2.9	0.082
Tagliafico et al.(³²32 Tagliafico A, Cadoni A, Fisci E, et al. Reliability of side-to-side ultrasound cross-sectional area measurements of lower extremity nerves in healthy subjects. Muscle Nerve. 2012;46:717-22.)	80	8.2	2.3	< 0.001	80	5.9	3.0	0.344	-	-	-	-	120	11.4	8	0.072
Current study	132	6.3	1.9	-	132	6.2	1.6	-	132	5.6	1.7	-	132	10	3.7	-

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[1] Correspondence: Dr. Marco Andrey Cipriani Frade. Serviço de Dermatologia, Departamento de Clínica Médica - FMRP-USP. Avenida Bandeirantes, 3900, Monte Alegre. Ribeirão Preto, SP, Brazil, 14049-900. Email: mandrey@fmrp.usp.br.