Characteristics of retrobulbar blood flow according to ultrasonic Doppler data in normal conditions

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INTRODUCTION

Ultrasound Doppler imaging (USDG) is one of the methods or registering changes in the retrobulbar flood flow. However, the method has not gained much prevalence in clinical practices. The main problems are the scarcity of theoretical and experimental knowledge, lack of clear qualitative and quantitative criteria of the norm and the pathology, whose values depend on the researcher and the sample, moreover, sometimes contradicting results of measurements are provided [1–5].

AIM

To establish reference characteristics of blood flow in the retrobulbar vessels and angular artery of the eye based on ultrasound Doppler imaging data in healthy people.

MATERIAL AND METHODS

USDG of retrobulbar blood vessels was performed for a group of volunteers on the base of the Chair of Diagnostic Radiology and Radiotherapy of the Donetsk State medical University. The group included healthy individuals. Thirty-six individuals (72 eyes) were examined, including 15 men (42%) and 21 women (58%), median age (М ± σ): 37.9 ± 14.7 years. Systolic arterial blood pressure and diastolic arterial blood pressure were measured with a manual blood pressure monitor on the brachial artery.

The examination was performed using the Toshiba Viamo SSA 640A unit using a linear probe with the frequency of 5–11 MHz. The probe set-up was compliant with safety criteria. Voluntary informed consent was obtained from the volunteers. The examination was performed with the patient in the supine position with eyes closed. The probe was positioned in the area of the eye socket and on the upper lid in multiple positions. The dimensions of the eye were measured in the B-mode: anteroposterior dimension (APD), anterior chamber depth (ACD), posterior corneal thickness (PCT), optic nerve thickness (ONT). Pulsed-wave Doppler ultrasound was used to obtain the spectral waveform. The spectral envelope was traced manually. Blood flow parameters were studied in the ophthalmic artery (OА), central retinal artery (CRA), posterior short ciliary arteries (PCA) on the temporal side, ophthalmic angular artery (AngA), central retinal vein (CRV). The following parameters were obtained: peak systolic blood flow velocity (PSV), end diastolic blood flow velocity (EDV), resistance index (RI), time-averaged maximum velocity over one cycle (TAMAX), pulsation index (PI), time of systolic acceleration (AccT). RI was calculated as [RI = (PSV - EDV) / PSV]. PI, as well as TAMAX, was calculated by the machine using the formula PI [PI = PSV / TAMAX]. For CRV, instead of PSV and EDV the maximum and minimum velocities of the blood flow were used (Vmax and Vmin). The study method also included locating the OA parallel to the posterior wall of the eye socket. Measurements in the CRA were taken 2–7 mm off the disk of the optic nerve. The spectral waveform of the CRV was registered on the same spectrogram as the CRA. Measurement of PCA was performed on the temporal side of the ocular bulb at the level of 2–7 posteriorly from the posterior contour of the eye, in the area close to the optic nerve. Localization of the AngA was performed in the upper medial angle of the eye socket, where the artery went deep into the eye socket. The AccТ was identified as the time from the onset of acceleration of systolic flow velocity to the maximum peak value. Visual analysis of the curve of the spectral waveform of the blood flow was performed with indication of the waveform type.

Statistical processing was performed using the standard statistical data processing software suite STATISTICA 10.0 (StatSoft, Inc., USA). The analysis of data obtained in the examinations involved generally accepted methods of basic mathematical statistics [6]. The statistical processing of medical and biological data involved the basic methods of mathematical statistics: descriptive statistics, pairwise and groupwise comparisons. A compulsory stage of results processing was the analysis of the sampling distribution to test their deviation from the normality using the Shapiro – Wilk's W-test (for n < 30) and Pearson's chi-square test (for n ≥ 30). For pairwise comparisons of sample groups, parametric tests (Student's t-test and Fisher's F-test) were used when the distribution followed a normal law. When the distribution deviated from normality, non-parametric tests (Wilcoxon W- and T-tests, and Pearson's chi-square test) were applied. In all cases, the critical significance level was set at 0.05. To assess the strength of association between pairs of variables, Pearson's correlation coefficient was used when the variables were normally distributed, and Spearman's rank correlation coefficient was applied when the distribution deviated from normality.

RESULTS

The data presented in Tables 1-4 were obtained in the examinations.

 

Table 1. Eye parameters in B-mode (M ± σ)

Таблица 1. Параметры глаза в В-режиме (М ± σ)

Parameter	APD, mm	ACD, mm	PCT, mm	ONT, mm
Value	24.2 ± 1.2	3.1 ± 0.4	0.89 ± 0.14	3.4 ± 0.5

 

Table 2. Blood flow characteristics (M ± σ) in retrobulbar vessels

Таблица 2. Характеристики кровотока (М ± σ) в ретробульбарных сосудах

Parameter	ОА	CRA	CRV	PCA	AngA
PSV, cm/s	23.4 ± 6.2	10.3 ± 2.9	4.5 ± 1.8	13.3 ± 5.7	17.2 ± 5.8
EDV, cm/s	6.4 ± 2.9	2.5 ± 1.2	2.5 ± 1.2	4.0 ± 2.5	4.6 ± 2.0
RI	0.73 ± 0.09	0.76 ± 0.08	0.45 ± 0.11	0.70 ± 0.10	0.73 ± 0.09
TAMAX, cm/s	11.1 ± 4.0	4.9 ± 1.6	-	7.3 ± 3.7	7.8 ± 2.9
PI	1.63 ± 0.53	1.64 ± 0.48	-	1.30 ± 0.34	1.71 ± 0.60
AccT, s	0.055 ± 0.008	0.054 ± 0.008	-	0.056 ± 0.007	0.055 ± 0.007

 

Table 3. Blood flow characteristics (M ± σ) in retrobulbar vessels in men and women

Таблица 3. Характеристики кровотока (М ± σ) в ретробульбарных сосудах у мужчин и женщин

Indicator	Men (n = 30)	Women (n = 42)	Statistical significance, р
Age	39.1 ± 16.0	37.1 ± 13.6	W = 1069.0, p = 0.766
ABP, mmHg	117.7 ± 9.3	117.4 ± 6.4	W = 1067.0, p = 0.740
DBP, mmHg	76.1 ± 5.8	74.9 ± 7.3	W = 1018.0, p = 0.335
APD, mm	24.2 ± 1.1	24.2 ± 1.3	W = 1062.0, p = 0.706
ACD, mm	3.2 ± 0.4	3.1 ± 0.4	W = 986.5, p = 0.213
PCT, mm	0.91 ± 0.14	0.89 ± 0.13	W = 958.0, p = 0.105
ONT, mm	3.4 ± 0.6	3.4 ± 0.5	T = 0.17, p = 0.865
PSV AO, cm/s	21.7 ± 5.6	23.4 ± 6.9	T = 1.81, p = 0.075
EDV AO, cm/c	5.7 ± 2.4	6.7 ± 3.1	T = 1.60, p = 0.114
RI AO	0.74 ± 0.09	0.74 ± 0.09	T = 0.17, p = 0.865
TAMAX AO, cm/s	10.0 ± 3.2	11.9 ± 4.3	W = 938.5, p = 0.074
PI AO	1.61 ± 0.55	1.64 ± 0.53	T = 0.19, p = 0.850
AccТ AO, s	0.055 ± 0.008	0.055 ± 0.007	W = 1072.0, p = 0.775
PSV CRA, cm/c	9.8 ± 2.5	10.8 ± 3.1	W = 963.5, p = 0.133
EDV CRA, cm/c	2.4 ± 1.2	2.6 ± 1.2	W = 1033.0, p = 0.475
RI CRA	0.75 ± 0.08	0.76 ± 0.07	W = 1089.0, p = 0.941
TAMAX CRA, cm/c	4.8 ± 1.5	5.0 ± 1.7	W = 1068.0, p = 0.758
PI CRA	1.56 ± 0.48	1.70 ± 0.47	T = 1.27, p = 0.208
AccТ CRA, s	0.056 ± 0.008	0.053 ± 0.007	W = 979.5, p = 0.153
Vmax CRV, cm/c	4.3 ± 1.5	4.6 ± 2.0	T = 0.78, p = 0.438
Vmin CRV, cm/c	2.3 ± 0.9	2.6 ± 1.3	W = 1053.0, p = 0.627
RI CRV	0.45 ± 0.11	0.44 ± 0.11	W = 1064.0, p = 0.723
PSV PCA, cm/c	13.2 ± 5.4	13.3 ± 5.9	W = 1085.0, p = 0.905
EDV PCA, cm/c	4.1 ± 2.0	3.9 ± 2.9	W = 1021.0, p = 0.398
RI PCA	0.69 ± 0.09	0.71 ± 0.10	T = 1.11, p = 0.271
TAMAX PCA, cm/c	7.3 ± 3.3	7.3 ± 4.0	W = 1078.0, p = 0.846
PI PCA	1.29 ± 0.36	1.31 ± 0.34	T = 0.26, p = 0.796
AccТ PCA, s	0.056 ± 0.008	0.055 ± 0.006	W = 1077.0, p = 0.818
PSV AngA, cm/c	17.9 ± 5.5	16.6 ± 6.0	T = 0.93, p = 0.356
EDV AngA, cm/c	4.8 ± 2.0	4.4 ± 2.0	T = 0.96, p = 0.340
RI AngA	0.73 ± 0.07	0.73 ± 0.11	T = 0.37, p = 0.713
TAMAX AngA, cm/c	8.2 ± 3.1	7.6 ± 2.8	T = 0.86, p = 0.393
PI AngA	1.71 ± 0.47	1.71 ± 0.68	T = 0.02, p = 0.984
AccТ AngA, s	0.055 ± 0.008	0.056 ± 0.006	W = 1055.0, p = 0.610

 

Table 4. Blood flow characteristics (M ± σ) in the retrobulbar vessels in the right and left eyes

Таблица 4. Характеристики кровотока (М ± σ) в ретробульбарных сосудах в правом и левом глазах

Indicator	Right eye (n = 36)	Left eye (n = 36)	Statistical significance, р
APD, mm	24.2 ± 1.0	24.2 ± 1.4	W = 1262.0, p = 0.558
ACD, mm	3.1 ± 0.4	3.1 ± 0.4	T = 0.27, p = 0.788
PCT, mm	0.90 ± 0.14	0.89 ± 0.13	W = 1305.0, p = 0.916
ONT, mm	3.4 ± 0.5	3.3 ± 0.5	T = 0.53, p = 0.598
PSV AO, cm/s	23.2 ± 6.6	23.4 ± 6.6	T = 0.10, p = 0.921
EDV AO, cm/s	6.2 ± 2.8	6.4 ± 2.9	W = 1298.0, p = 0.857
RI AO	0.74 ± 0.08	0.73 ± 0.09	T = 0.45, p = 0.654
TAMAX AO, cm/s	10.8 ± 3.9	11.4 ± 4.2	T = 0.64, p = 0.524
PI AO	1.62 ± 0.49	1.63 ± 0.58	W = 1211.0, p = 0.244
AccТ AO, s	0.054 ± 0.007	0.056 ± 0.008	W = 1244.0, p = 0.392
PSV CRA, cm/s	10.0 ± 3.2	10.7 ± 2.6	W = 1198.0, p = 0.260
EDV CRA, cm/s	2.2 ± 0.9	2.8 ± 1.4	W = 1147.0, p = 0.060
RI CRA	0.77 ± 0.09	0.75 ± 0.08	W = 1167.0, p = 0.096
TAMAX CRA, cm/s	4.6 ± 1.4	5.2 ± 1.8	W = 1178.0, p = 0.124
PI CRA	1.72 ± 0.49	1.56 ± 0.45	T = 1.36, p = 0.178
AccТ CRA, s	0.054 ± 0.008	0.054 ± 0.007	W = 1278.0, p = 0.661
Vmax CRV, cm/s	4.7 ± 2.1	4.2 ± 1.4	T = 1.12, p = 0.267
Vmin CRV, cm/s	2.6 ± 1.4	2.3 ± 0.9	W = 1244.0, p = 0.427
RI CRV	0.45 ± 0.11	0.44 ± 0.11	T = 0.25, p = 0.803
PSV PCA, cm/s	13.9 ± 6.0	12.2 ± 4.8	W = 1198.0, p = 0.260
EDV PCA, cm/s	4.5 ± 3.2	3.4 ± 1.5	W = 1180.0, p = 0.182
RI PCA	0.69 ± 0.12	0.71 ± 0.07	W = 1221.0, p = 0.649
TAMAX PCA, cm/s	7.8 ± 4.2	6.6 ± 2.7	W = 1194.0, p = 0.238
PI PCA	1.28 ± 0.41	1.33 ± 0.28	W = 1199.0, p = 0.483
AccТ PCA, s	0.056 ± 0.007	0.055 ± 0.007	W = 1254.0, p = 0.585
PSV AngA, cm/s	17.4 ± 5.4	16.9 ± 6.2	T = 0.39, p = 0.698
EDV AngA, cm/s	4.5 ± 2.0	4.6 ± 2.0	T = 0.12, p = 0.905
RI AngA	0.74 ± 0.09	0.72 ± 0.10	T = 0.77, p = 0.444
TAMAX AngA, cm/s	8.0 ± 2.8	7.7 ± 3.0	T = 0.32, p = 0.750
PI AngA	1.72 ± 0.60	1.69 ± 0.61	T = 0.18, p = 0.858
AccТ AngA, s	0.055 ± 0.007	0.055 ± 0.007	W = 1212.0, p = 0.203

 

No statistically significant difference of indicators was found between the right and the left eye (p > 0.05). No statistically difference of indicators was found between men and women (p > 0.05). In pairwise correlations (Kendall test), the correlation between the age and parameters of the eye was not identified in B-mode (R = 0, p > 0.05), correlation between the age and characteristics of blood flow was not identified (R = 0, p > 0.05).

In B-mode, the media of the vitreum were homogenous, the echo-structure of the crystalline was normal (homogenous except the half hemisphere of the posterior contour), the optic disc was not displaced.

In the analysis of the blood flow spectrum, all vessels demonstrated a main unchanged type of blood flow, characterized by a ‘sharp' systolic peak, the presence of a dicrotic notch (reaching the level of the isoline, below and above it) and the presence of undulating diastolic blood flow with sharp peaks (2–4 peaks following the dicrotic notch). The acceleration time (AccT) did not exceed 0.08 s (Figs. 1, 2).

 

Figure 1. Main unchanged blood flow spectrum in the OA.

Рисунок 1. Магистральный неизмененный спектр кровотока в ОА.

 

Figure 2. Main unchanged blood flow spectrum in the AngA.

Рисунок 2. Магистральный неизмененный спектр кровотока в AngA.

 

DISCUSSION

In comparison with data of studies of other authors [5, 7–15], in this study the blood flow velocities were lower, especially in the ОА. The lower velocity in the OA may be explained by different functional states, but it is more likely that this stems from specific features of the hardware and presets of choice. It is known that USDG of retrobulbar vessels does not provide data on the vessel diameter and evaluates only the linear velocity of the blood flow, while the volumetric velocity may be comparable. This suggestion may be supported by the difference of blood flow values between the right and the left eyes of the same individuals, which could have been two-fold, without any statistically significant difference in our sample [1, 5, 16–19].

The differences in hemodynamics dependent on auto-regulation, and non-fixed number of collaterals of the PCA may yield a significant difference of normal linear velocities of blood flow. The combined use of spectral and numeric characteristics may provide higher diagnostic accuracy of disorders; however, at the moment it is not used neither in scientific nor in routine research. This might explain the discrepancy in the blood flow parameters reported by other authors who assessed the changes in the blood flow in pathological conditions. Confirmation of this hypothesis will necessitate studies in groups with pathologies [2, 4–6].

In our opinion, the spectral waveform of the blood flow in the retrobulbar vessels differs from classic interpretations of high- and low-resistant blood flow, mono-, bi- and tri-phase blood flow. Retrobulbar vessels are also devoid of the risk of velocity change due to compression with the probe. Literature provides few descriptions of the spectral waveform of the retrobulbar vessels. They all describe flattening of the spectral waveform line or the loss of the diastolic spectrum [11, 19–21]. Maintenance of diastolic perfusion pressure requires the availability of a diastolic blood flow; therefore, the retrobulbar vessels will have a lower RI in normal conditions than the vessels of the extremities. In our sample, the diastolic spectrum was registered in all vessels [12, 14, 22–27].

We were not able to find assessment of AngA in open sources, the importance of this vessel for the hemodynamics of the eye has not been assessed before; the anastomosis may be used in compensatory changes in ischemic processes of the eye and the brain (compensation of blood flow in the middle cerebral artery via the ophthalmic artery).

CONCLUSION

We presented the findings on reference blood flow obtained in USDG of retrobulbar vessels in healthy individuals. We performed a visual analysis of the spectral waveform of the blood flow obtained by pulse-wave Doppler imaging and recorded characteristics of the normal spectrum of the blood flow. For the first time, reference parameters of the AngA blood flow were presented. Combined use of spectral and numeric characteristics may potentially have higher diagnostic accuracy, which may improve the informative value of the method.

 

ADDITIONAL INFORMATION	ДОПОЛНИТЕЛЬНАЯ ИНФОРМАЦИЯ
Ethics approval. The study adhered to the ethical principles of the World Medical Association. The study was approved by the Biomedical Ethics Committee of the M. Gorky Donetsk State Medical University (extract from meeting minutes No. 59/5-1 dated October 26, 2023). Informed consent was obtained from all study participants.	Этическая экспертиза. В работе соблюдались этические принципы, предъявляемые Хельсинкской декларацией Всемирной медицинской ассоциации. Исследование одобрено комитетом по биомедицинской этике при ФГБОУ ДонГМУ им. М. Горького (выписка из протокола заседания №59/5-1 от 26.10.2023). Информированное согласие получено от всех участников исследования.
Study funding. The study was the authors' initiative without external funding.	Источник финансирования. Работа выполнена по инициативе авторов без привлечения финансирования.
Conflict of interest. The authors declare that there are no obvious or potential conflicts of interest associated with the content of this article.	Конфликт интересов. Авторы декларируют отсутствие явных и потенциальных конфликтов интересов, связанных с содержанием настоящей статьи.
Contribution of individual authors. Vakulenko I.P., Fominov V.M.: scientific supervision, development of the study concept, consulting on radiation diagnostics, final text revision, final conclusions. Zolotukhin A.S.: development of the study concept, implementation of the study, writing of the text. All authors gave their final approval of the manuscript for submission, and agreed to be accountable for all aspects of the work, implying proper study and resolution of issues related to the accuracy or integrity of any part of the work.	Участие авторов. Вакуленко И.П., Фоминов В.М.: научное руководство, разработка концепции исследования, консультирование по вопросам лучевой диагностики, доработка текста, итоговые выводы. Золотухин А.С.: разработка концепции исследования, выполнение исследований, написание текста. Все авторы одобрили финальную версию статьи перед публикацией, выразили согласие нести ответственность за все аспекты работы, подразумевающую надлежащее изучение и решение вопросов, связанных с точностью или добросовестностью любой части работы.
Statement of originality. No previously published material (text, images, or data) was used in this work.	Оригинальность. При создании настоящей работы авторы не использовали ранее опубликованные сведения (текст, иллюстрации, данные).
Data availability statement. The editorial policy regarding data sharing does not apply to this work.	Доступ к данным. Редакционная политика в отношении совместного использования данных к настоящей работе не применима.
Generative AI. No generative artificial intelligence technologies were used to prepare this article.	Генеративный искусственный интеллект. При создании настоящей статьи технологии генеративного искусственного интеллекта не использовали.
Provenance and peer review. This paper was submitted unsolicited and reviewed following the standard procedure. The peer review process involved 2 external reviewers.	Рассмотрение и рецензирование. Настоящая работа подана в журнал в инициативном порядке и рассмотрена по обычной процедуре. В рецензировании участвовали 2 внешних рецензента.

About the authors

I. P. Vakulenko

Donetsk State Medical University named after M. Gorky

Email: vakulenko.i.p@gmail.com
ORCID iD: 0009-0000-7987-3768

MD, Dr. Sci. (Medicine), Head of the Department of Radiation Diagnostics and Radiation Therapy

Russian Federation, Donetsk

A. S. Zolotukhin

Donetsk State Medical University named after M. Gorky

Author for correspondence.
Email: mizerakl97@gmail.com
ORCID iD: 0009-0009-8950-0485

Postgraduate Student of the Department of the Radiation Diagnostics and Radiation Therapy

Russian Federation, Donetsk

V. M. Fominov

Donetsk State Medical University named after M. Gorky

Email: vitaliy.fominov@inbox.ru
ORCID iD: 0009-0009-5420-8302

MD, Cand. Sci. (Medicine), Associate Professor, Department of Radiation Diagnostics and Radiation Therapy

Russian Federation, Donetsk

References

Supplementary files