The role of testicular microcirculatory disorders in spermatogenic dysfunction in obese men

doi:10.21203/rs.3.rs-2343004/v1

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The role of testicular microcirculatory disorders in spermatogenic dysfunction in obese men

https://doi.org/10.21203/rs.3.rs-2343004/v1

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Background: Obesity is a recognized risk factor for systemic microcirculatory disorders. The association between obesity-related microcirculatory disorders and spermatogenesis has been difficult to investigate and has not been reported in the literature until now. The aim of this study was to study the role of testicular microcirculatory disorders in spermatogenic dysfunction in obese men.

Subjects: 576 participants were enrolled in this prospective observational study.

Methods: Angio PLUS^TM Planwave Ultrasensitive Imaging of the testicular microcirculation was performed and the number of vessels was counted and recorded as the ultrasonic microvascular density (UMVD).

Results: Participants were divided into Group I (normozoospermia), Group II (asthenozoospermia, teratozoospermia and asthenoteratozoospermia) and Group III (oligozoospermia and NOA) based on semen results. There were no differences in BMI and UMVD between semen groups (p>0.05). Participants were then divided into normal weight, overweight and obese subgroups based on body mass index. In the obese subgroup, UMVD tended to decrease with decreasing sperm concentration, with significant differences in groups I, II and III (p<0.01). ROC curve for UMVD was established for differential diagnosis between Groups I, II and Group III in the obese subgroup. UMVD had a high diagnostic value with a cut-off value of 19.25 /cm², AUC of 0.829, sensitivity of 0.773 and specificity of 0.737 (95% CI: 0.740-0.917).

Conclusions: Our findings suggest that microcirculatory disorders play an essential role in the development of spermatogenic dysfunction in obese men. Obese participants with oligozoospermia and NOA had a significantly lower UMVD. Testicular UMVD below 19.25 /cm²was highly suggestive of spermatogenic dysfunction. Angio PLUS^TM Planwave Ultrasensitive Imaging should be used routinely to screen testicular microcirculation in obese men and to identify those who may benefit from microcirculation improvement therapy.

Health sciences/Diseases/Endocrine system and metabolic diseases/Obesity

Health sciences/Signs and symptoms

male

microcirculation

obesity

testis

ultrasonography

The prevalence of obesity in China has increased rapidly in the past four decades. Based on Chinese criteria, the latest national prevalence estimates for 2015–2019 are 3.6% in children younger than six years, 7.9% in children and adolescents aged 6–17 years, and 16.4% in adults ( ≧ 18 years)¹. Experimental and observational evidence suggests that metabolic dysfunction associated with obesity can lead to male infertility^{2, 3}. Although obesity is increasingly recognized as a risk factor for male fertility, the impact of obesity on semen parameters and male fertility remains controversial^{4, 5}. Continued research in this area is necessary due to the inconsistency and severity of the potential consequences of obesity on male fertility.

Obesity is a recognized risk factor for systemic microcirculatory disorders. The association between obesity-related microcirculatory disorders and chronic disease has been the focus of ongoing research^{6, 7}. However, the association between obesity-related microcirculatory disorders and spermatogenesis has been difficult to investigate and has not been reported in the literature until now. Advances in ultrasound microvascular technologies have made it possible to study testicular microcirculation in obese men.

Ultrasound microvascular technologies include Superb microvascular imaging (SMI) and Angio PLUS™ Planwave Ultrasensitive Imaging (AP).

SMI has found its way into routine applications since 2014. It can improve the detectability of slow or small-vessel flow signals by using specific filters and can provide information on blood flow in vessels bigger than 100 µm in diameter. SMI has been widely used in evaluating tumor neovascularization⁸. In recent years, several scholars have attempted to detect microcirculation to indirectly assess the function of organs or the severity of diffuse diseases^9–11. SMI has also been used to assess testicular perfusion and has achieved good diagnostic efficacy. In the paediatric testis, conventional color Doppler flow imaging (CDFI) is difficult to detect intra-testicular blood flow, but SMI can obtain additional blood flow information¹². SMI can also be used to detect testicular microvascularity in children with early-stage scrotal pain, cryptorchidism and inguinal hernia^13–15. In the adult testis, SMI can quantify impaired testicular microcirculation on the side of the varicocele and can be used effectively in the diagnosis and follow-up of testicular microvascular injury¹⁶.

In recent years, AP is a more advanced approach to microvascular imaging. It relies on two core technologies, unfocused or plane waves and three-dimensional wall filtering. It can provide a new level of microvascular imaging with significant improvements in color sensitivity and spatial resolution, and can maintain excellent two-dimensional imaging and eliminate significant motion artifacts ^{17, 18}. AP can provide information on blood flow in vessels larger than 50 µm in diameter and is well-suited for assessing testicular microcirculation.

The aim of this study was therefore to elucidate the relationship between microcirculatory disorders and spermatogenic dysfunction associated with obesity and to identify obese patients who might benefit from microcirculatory improvement therapies.

Participant screening and enrollment

This prospective observational study was conducted according to the Declaration of Helsinki for Medical Research involving Human Subjects and was approved by the Ethics Committee of Shengjing Hospital of China Medical University (NO.2020PS123J). Written informed consent was obtained from all participants before participating in this study. Before commencing the study, we estimated a total study size of 849 participants allowed for a power (1-abeta) of 90% at a significance level of 0.01 and a dropout rate of 30%. Initially, a total of 912 consecutive participants who visited the Reproductive Medicine center of our hospital between December 2020 and December 2021 were enrolled. To reduce selection bias, strict inclusion and exclusion criteria were set before the study.

The inclusion criteria were as follows: (I) scrotal ultrasound and AP examination were performed; (II) semen analysis was completed within seven days following the ultrasound examination.

The exclusion criteria were as follows: (I) abnormal ultrasound findings, including testicular masses, cryptorchidism, varicocele, extensive microlithiasis, hydrocele, solitary testis and inguinal hernia; (II) factors affecting ejaculation, including retrograde ejaculation, history of urethral reconstruction surgery and obstructive azoospermia (OA); (III) radiotherapy or chemotherapy had been carried out within the past two years; (IV) history of testicular trauma; (V) testicular biopsy had been performed within the past three months; (VI) severe chronic diseases or metabolic disorders, including hypertension, diabetes, metabolic syndrome and severe chronic renal or hepatic diseases; (VII) chromosomal abnormalities; (VIII) satisfactory images were unobtainable (for various reasons).

Instruments and Methods

The AP examination was performed using an ultrasound diagnostic imaging system Aixplorer (SuperSonic Imagine, Aix en Provence, France) and a linear transducer operating at the frequency of 4–15 MHz. The scrotal ultrasound and AP examination were performed by an experienced radiologist with more than five years of experience in scrotal ultrasound.

All participants were examined in the supine position. A grayscale ultrasound of the scrotum was performed first. The scrotal contents were examined, and the placement, contour, size, and parenchymal echo of the testes were determined. Testicular length, width, and height were measured and testicular volume was calculated with the formula of Lambert: testicular volume (mL) = (length × width × height) × 0.71¹⁹. The Volume-mean was defined as the average volume of the testes bilaterally.

For the AP examination, a grey-scale image was first obtained in the largest longitudinal plane of the testis. The AP examination was then performed at a section perpendicular to the centripetal arteries. The area of detection included the entire section. In the absence of noise, the gain setting was adjusted to the optimum. During the AP examination, the participants were asked to hold their breath and no pressure was applied through the transducer to prevent the vessels from collapsing. Images of clearly detectable microvessels were stored as shown in Fig. 1. The stored images were observed independently by two experienced radiologists. An area of 1 cm² in the center of the testis with the richest microvascularity was selected and the number of vessels was counted by each of the two radiologists. The average number of vessels in both testes was recorded as the ultrasonic microvascular density (UMVD, /cm²). The mean UMVD counted by the two radiologists was then recorded as the UMVD-mean for subsequent statistical analysis.

Body mass index (BMI) calculation

The measurements of weight and height were taken by the nurses. BMI was calculated as weight (kg) divided by height squared (m²).

Patient grouping according to BMI

BMI was categorized as underweight (BMI < 18.5), normal weight (18.5 ≦ BMI < 25), overweight (25 ≦ BMI < 30), and obese (BMI ≧ 30) (Centers for Disease Control and Prevention Overweight and obesity). All participants were grouped according to BMI.

Semen collection and analysis

Semen samples were collected by masturbation in semen collection chambers after 3–7 days of abstinence. Then they were evaluated according to the guideline established by the World Health Organization (WHO) in 2010.

Patient grouping according to semen results

The basic semen testing procedures in the sixth edition are consistent within the fifth edition. Participants were therefore grouped into three groups based on semen results according to the WHO criteria for 2021 (WHO Laboratory Manual for the Examination and Processing of Human Semen, 6th edition).

Group I: Normal control group, normozoospermia (semen volume ≧ 1.4 mL, sperm concentration ≧ 16×10⁶/mL, progressive motility ≧ 30% and normal form sperm morphology ≧ 4%);

Group II: Asthenozoospermia, teratozoospermia, and asthenoteratozoospermia (semen volume ≧ 1.4 mL, sperm concentration ≧ 16×10⁶/mL, progressive motility ≦ 30%, or progressive + non-progressive motility < 42%, and/or normal form sperm morphology ≦ 4%);

Group III: Oligozoospermia (sperm concentration < 16×10⁶/mL) and non-obstructive azoospermia (NOA).

Statistical analysis

Statistical analysis was performed using SPSS 25.0 (IBM SPSS Statistics for Windows, Version 25.0. Armonk, NY: IBM Corp.). Data were tested for normality using the Kolmogorov-Smirnov normality test. The data did not conform to a normal distribution and was presented as the median and first and third quartiles. The intraclass correlation coefficient (ICC) was used to assess the interobserver agreement of UMVD. Statistical differences between two groups were identified using the Mann-Whitney U test and between three or more groups using the Kruskal-Wallis test. The receiver operating characteristic (ROC) curve was estimated to assess the predictive value for UMVD in the differential diagnosis between Group I, II, and Group III obese participants. The area under the ROC curve (AUC), sensitivity, and specificity were calculated, and the cut-off value was determined by the Youden index. p < 0.05 indicated a statistically significant difference.

Participants screening and enrollment

The screening and enrollment of participants are illustrated in Fig. 2. A total of 576 participants were enrolled in the study, and 336 were excluded.

Inter-observer agreement for UMVD

Good agreement regarding the counting of UMVD was seen between the two observers with the intraclass correlation coefficient (ICC) value of 0.812 (95% CI: 0.782–0.838, p < 0.01).

Age, sperm concentration, volume-mean, BMI and UMVD in different semen groups

Age, sperm concentration, Volume-mean, BMI and UMVD for different semen groups are shown in Table 1. There were no significant differences in BMI and UMVD between Groups I, II and III (p > 0.05). Volume-mean values decreased with decreasing sperm concentration and were significantly different between groups (p < 0.01). There was a significant difference in age between groups (p < 0.01), but a significant overlap of individual values was observed.

Table 1

Age, sperm concentraion, Volume-mean, BMI and UMVD in different semen groups.
Item	Group I (n = 198)	Group II (n = 266)	Group III (n = 112)	p
Age	32* (29,36)	33 (31,36)	32 (29, 35)	p < 0.01
Sperm concentration	62.72 (43.87,89.77)	40.33 (27.96,62.86)	0 (0,6.27)	-
Volume-mean	14.74 (12.41,17.25)	13.87 (12.19,16.06)	8.89 (5.45,12.44)	p < 0.01
BMI	26.30 (24.30,28.48)	26.40 (23.70,28.40)	25.85 (23.95,28.63)	p = 0.851
UMVD-mean	24.00 (20.00,27.50)	25.00 (21.38,29.00)	24.25 (18.00,29.88)	p = 0.194
*, median and first and third quartiles; UMVD, ultrasonic microvessel density; BMI, body mass index; Group I, participants with normozoospermia; Group II, participants with asthenozoospermia, teratozoospermia and asthenoteratozoospermia; Group III, participants with oligozoospermia and non-obstructive azoospermia.

Age, sperm concentration, Volume-mean and UMVD in different BMI subgroups

One male with a BMI of 16.9 was excluded from the analysis. Age, sperm concentration, Volume-mean and UMVD for the different BMI subgroups are demonstrated in Table 2. There were significant differences in volume-mean (p < 0.05) and UMVD (p < 0.01) between the different BMI subgroups, but there was a significant overlap of individual values between the subgroups.

Table 2

Age, sperm concentraion, Volume-mean and UMVD in different BMI groups.
Item	18.5 ≦ BMI < 25 (n = 208)	25 ≦ BMI < 30 (n = 273)	BMI ≧ 30 (n = 94)	p
Age	33* (30,37)	33 (30,35)	32.5 (29, 36)	p = 0.212
Sperm concentration	41.18 (20.60,69.32)	41.00 (21.76,69.11)	36.27 (20.05,62.98)	p = 0.572
Volume-mean	13.15 (10.81,15.59)	13.99 (11.19,16.15)	13.86 (11.24,17.56)	p < 0.05
BMI	23.10 (22.10,24.30)	26.80 (26.20,27.90)	32.40 (31.20,34.60)	-
UMVD-mean	24.50 (20.50,29.00)	25.00 (21.00,29.25)	22.00 (18.00,26.00)	p < 0.01
*, median and first and third quartiles; UMVD, ultrasonic microvessel density; BMI, body mass index.

Age, Volume-mean, and UMVD of Group I, Group II and Group III in different BMI subgroups

Age, volume-mean and UMVD of Group I, Group II and Group III in different BMI subgroups are shown in Table 3. Within each BMI subgroup, there was a significant difference (P < 0.01) in the Volume-mean for Groups I, II and III. However, no statistically significant difference was observed for age (P > 0.05). In the normal weight subgroup, UMVD tended to increase as sperm concentration decreased, with statistically significant differences in Groups I, II and III (p < 0.05). In the overweight subgroup, there was no statistical difference in UMVD between Groups I, II and III (p > 0.05). In the obese subgroup, UMVD tended to decrease as sperm concentration decreased, with statistically significant differences in Groups I, II and III (p < 0.01).

Table 3

Age, Volume-mean, and UMVD of Group I, Group II and Group III in different BMI groups.
Item	Semen Group	N	Age	UMVD-mean	Volume-mean
18.5 ≦ BMI < 25 (n = 208)	Group I	65	33* (30,38)	23.00 (19.25,26.25)	13.98 (11.99,16.48)
	Group II	99	34 (31,37)	25.50 (21.50,29.00)	13.52 (11.98,15.93)
	Group III	44	31 (28,34.75)	28.75 (18.25,32.75)	8.31 (5.21,11.88)
	p	-	< 0.05	< 0.05	< 0.01
25 ≦ BMI < 30 (n = 273)	Group I	99	32 (30,35)	24.50 (21.00,28.50)	15.20 (13.21,17.45)
	Group II	125	33 (30,36)	25.50 (21.50,29.50)	13.92 (12.20,15.97)
	Group III	49	32 (29,34)	25.00 (20.25,29.50)	8.99 (5.75,13.59)
	p	-	< 0.05	0.517	< 0.01
BMI ≧ 30 (n = 94)	Group I	33	31 (28,36)	24.00 (20.25,26.50)	15.51 (12.27,18.03)
	Group II	42	32 (31,35.25)	22.75 (18.88,26.00)	14.56 (12.50,18.62)
	Group III	19	35 (29,37)	17.00 (12.50,20.50)	9.18 (5.42,13.87)
	p	-	0.429	< 0.01	< 0.01
*, median and first and third quartiles; UMVD, ultrasonic microvessel density; BMI, body mass index; Group I, participants with normozoospermia; Group II, participants with asthenozoospermia, teratozoospermia and asthenoteratozoospermia; Group III, participants with oligozoospermia and non-obstructive azoospermia.

ROC curve of UMVD

There were 94 participants in the obese subgroup. The ROC curve of UMVD for differential diagnosis between participants in Groups I, II and III is shown in Fig. 1. UMVD had a high diagnostic value with a cut-off value of 19.25 /cm², AUC of 0.829, sensitivity of 0.773, and specificity of 0.737 (95% CI: 0.740–0.917, p < 0.01).

In this study, participants were first grouped according to their semen results, and comparisons of UMVD in each semen group showed no significant differences. This result suggests that even if the spermatogenic function is severely impaired, the vast majority of participants do not experience microcirculatory disturbances. Microcirculatory disorders are not determinants of the onset and progression of spermatogenic dysfunction. To analyze the effect of obesity on testicular microcirculation, we grouped participants by BMI and found that the UMVD was significantly lower in obese participants than in normal weight and overweight participants. This result suggests that obesity has a negative effect on testicular microcirculation. To analyze the effect of obesity-induced testicular microcirculatory disorders on spermatogenesis, we analyzed the UMVD in groups I, II and III in each BMI group. We did not find significant microcirculatory disorders in either normal weight or overweight participants, even though these participants had severe oligozoospermia and NOA. However, in the obese subgroup, participants with asthenozoospermia, teratozoospermia and asthenoteratozoospermia began to show mild microcirculatory disorders, while participants with oligozoospermia and azoospermia showed a significant decrease in UMVD. All of this suggests that microcirculatory disorders play a crucial role in the development and progression of spermatogenic dysfunction in obese participants.

Obesity is closely associated with hyperglycemia and disorders of lipid metabolism^{20, 21}. The vast majority of obese adults have metabolic syndrome and diabetes. Metabolic syndrome is a cluster of obesity-related cardiovascular risk factors, including abdominal obesity, impaired glucose tolerance, dyslipidemia, and elevated blood pressure²⁰. In contrast, systemic metabolic abnormalities, such as hyperglycemia, hypertension and dyslipidemia, have varying degrees of negative impact on microcirculation²². Therefore, studies aimed at identifying microcirculatory disorders associated with obesity should be performed on participants with uncomplicated obesity. Unfortunately, the data available from this particular group of obese adults is extremely limited. In this study, the participants enrolled ranged in age from 19 to 62 years (mean, 33.20 years; median, 33 years), with the majority of them between 25 and 35 years of age. Because the participants were relatively young and a high proportion of obese participants were uncomplicatedly obese, we excluded participants with metabolic syndrome and diabetes and included only uncomplicatedly obese participants to provide more accurate data on the effects of obesity on testicular microcirculation.

Obesity is a recognized risk factor for systemic microvascular dysfunction. It typically leads to a significantly increased risk of fatty liver, reduced exercise tolerance, microvascular dementia, myocardial ischemia, hypertension, proteinuria, and impaired glucose tolerance^{23, 24}. Obesity affects the microcirculation of tissues in two ways. First, changes in microvascular morphology and function caused by obesity lead to microvascular rarefaction^25–27. In addition, elevated plasma viscosity due to obesity decreases microvascular blood flow velocity. In obese adults, elevated plasma viscosity is most likely due to dyslipidemia, reduced erythrocyte deformation or erythrocyte aggregation due to triglycerides^{28, 29}. The combination of microvascular rarefaction and hemorheological abnormalities in obese patients leads to impaired microcirculation, which is manifested by a reduction in UMVD. Microcirculation has different roles in a variety of highly specialized tissues. Although obesity can cause systemic microcirculatory disorders, the effects of obesity on microcirculation manifest differently in each organ and have different clinical implications²³. The microcirculatory changes in diabetes mellitus and non-obstructive coronary ischemia have now been intensively studied and their diagnosis and treatment have been standardized in relevant guidelines^{22, 30}. However, spermatogenic dysfunction due to microcirculatory disorders associated with obesity has not received sufficient attention in clinical practice. Currently, there are no recognized validated methods for assessing testicular microcirculatory dysfunction in obese patients, nor are there standardized guidelines for diagnosis and treatment. More in-depth research is needed in this area.

The vascular structure of the testis has its characteristics. The testicular vessels pass superficially beneath the tunica albuginea, forming a vascular layer known as the tunica albuginea. The upper polar, mediastinum, and posterolateral segments of the testis surface are areas of abundant vascularity; The middle third of the lateral surface is the moderately vascular area³¹. For this reason, the central part of the testis was chosen as the area of interest during the examination. If the testis was small, try to avoid the richly vascularised areas mentioned above to obtain more accurate microvascular information. The three-dimensional structure of the microvasculature in the human testis has been described in detail in an anatomical study³². Numerous tiny branches of the testicular artery enter the parenchyma of the testis. These branches are centripetal arteries. They run in a relatively straight course within the testicular septa towards the rete testis and enter the recurrent arteries before the rete testis, usually accompanied by one or two large centrifugal or centripetal veins. From the branches of the recurrent arteries, the segmental arteries emerge at relatively regular intervals, averaging 300 µm, and then divide into capillaries. A centripetal artery is responsible for the blood supply to several lobules, a recurrent artery is responsible for one lobule, and a segmental artery is responsible for only one region of the seminiferous tubules³². Based on the shape and structure of the vessels in the testis, the vessels that can be detected by AP are the centripetal arteries, the centrifugal and centripetal veins, and some of the recurrent arteries. This suggests that it is feasible for the AP to assess the testicular microcirculation. We chose a section perpendicular to the centripetal arteries as the viewing and counting section, which would show more of the testicular vasculature and give a full picture of the state of the testicular microcirculation.

Ultrasound is the first-line screening strategy for scrotal diseases. AP is a current ultrasound microvascular imaging technique that does not require the use of contrast agents. It is easy to master and suitable for incorporation into routine clinical workflow. In this study, we found AP to be effective in assessing the microvascular status of the testis in obese men. A testicular UMVD of less than 19.25 /cm² in obese men is highly suggestive of spermatogenic dysfunction. The results of this study provide a basis for further accurate diagnosis and standardized treatment of testicular microcirculatory disorders in obese men.

This study has some shortcomings. First, as a new imaging technique, AP is highly sensitive to low-velocity blood flow. However, in the absence of contrast, AP cannot dynamically visualize blood flow in and out of the testis, nor can it adequately show the vascular structure and distribution of testicular capillaries. Ultra-low velocity blood flow cannot be visualized when the blood velocity is significantly below the velocity range recognized by the AP. If the color gain is increased excessively to observe ultra-low velocity blood flow, noise artifacts can occur. Second, the gold standard for assessing microvascular status is the pathological microvascular density. Harvesting testicular tissue from participants would not be ethical. Therefore, the UMVD derived from AP cannot be compared with histological microvascular densities. Finally, although the study included a large number of participants, the number of obese participants was relatively small. Further studies with larger sample sizes are needed.

This study showed that obese participants with oligozoospermia and NOA had a significantly lower UMVD. If the testicular UMVD in obese men was below 19.25 / cm², this was highly suggestive of spermatogenic dysfunction. Our findings suggest that microcirculatory disorders play an essential role in the development of spermatogenic dysfunction in obese men. AP should be used routinely to screen testicular microcirculation in obese men and to identify those who may benefit from microcirculation improvement therapy.

No conflict of interest to declare.

Competing Interests

The authors declare no competing interests

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Author Contributions

JC and S-ST conceived and carried out the experiments. JC and WF conceived the experiments and analyzed data. WF carried out experiments. All authors were involved in writing the paper and had final approval of the submitted and published versions.

Pan X-F, Wang L, Pan A. Epidemiology and determinants of obesity in China. The Lancet Diabetes & Endocrinology 2021; 9(6): 373–392.
Sallmen M, Sandler DP, Hoppin JA, Blair A, Baird DD. Reduced fertility among overweight and obese men. Epidemiology 2006; 17(5): 520–3.
Ramlau-Hansen CH, Thulstrup AM, Nohr EA, Bonde JP, Sorensen TI, Olsen J. Subfecundity in overweight and obese couples. Hum Reprod 2007; 22(6): 1634–7.
Eisenberg ML, Kim S, Chen Z, Sundaram R, Schisterman EF, Louis GM. The relationship between male BMI and waist circumference on semen quality: data from the LIFE study. Hum Reprod 2015; 30(2): 493–4.
McPherson NO, Tremellen K. Increased BMI 'alone' does not negatively influence sperm function - a retrospective analysis of men attending fertility treatment with corresponding liver function results. Obes Res Clin Pract 2020; 14(2): 164–167.
Boly CA, Venhuizen M, Dekker NAM, Vonk ABA, Boer C, van den Brom CE. Comparison of Microcirculatory Perfusion in Obese and Non-Obese Patients Undergoing Cardiac Surgery with Cardiopulmonary Bypass. J Clin Med 2021; 10(3).
Sukumaran V, Tsuchimochi H, Sonobe T, Waddingham MT, Shirai M, Pearson JT. Liraglutide treatment improves the coronary microcirculation in insulin resistant Zucker obese rats on a high salt diet. Cardiovasc Diabetol 2020; 19(1): 24.
Jiang ZZ, Huang YH, Shen HL, Liu XT. Clinical Applications of Superb Microvascular Imaging in the Liver, Breast, Thyroid, Skeletal Muscle, and Carotid Plaques. J Ultrasound Med 2019; 38(11): 2811–2820.
Balik AO, Kilicoglu ZG, Gormez A, Ozkara S. Radiology-pathology correlation in staging of liver fibrosis using superb microvascular imaging. Diagn Interv Radiol 2019; 25(5): 331–337.
Gao J, Thai A, Erpelding T. Comparison of superb microvascular imaging to conventional color Doppler ultrasonography in depicting renal cortical microvasculature. Clin Imaging 2019; 58: 90–95.
Bayramoglu Z, Kandemirli SG, Caliskan E, Yilmaz R, Kardelen AD, Poyrazoglu S et al. Assessment of paediatric Hashimoto's thyroiditis using superb microvascular imaging. Clin Radiol 2018; 73(12): 1059 e9-1059 e15.
Ayaz E, Ayaz M, Onal C, Yikilmaz A. Seeing the Unseen: Evaluating Testicular Vascularity in Neonates by Using the Superb Microvascular Imaging Ultrasound Technique. J Ultrasound Med 2019; 38(7): 1847–1854.
Visalli C, Vinci SL, Mondello S, Kobeissy F, Salamone I, Coglitore A et al. Microvascular imaging ultrasound (MicroV) and power Doppler vascularization analysis in a pediatric population with early scrotal pain onset. Jpn J Radiol 2022; 40(2): 192–201.
Keceli M, Keskin Z, Keskin S. Comparison of Superb Microvascular Imaging With Other Doppler Methods in Assessment of Testicular Vascularity in Cryptorchidism. Ultrasound Q 2020; 36(4): 363–370.
Seher N, Nayman A, Koplay M, Ciftci I. Comparison of Preoperative and Postoperative Testicular Elasticity and Vascularity in Pediatric Patients With Inguinal Hernia. J Ultrasound Med 2022; 41(1): 71–78.
Ates F, Durmaz MS, Sara HI, Kara T. Comparison of testicular vascularity via superb microvascular imaging in varicocele patients with contralateral normal testis and healthy volunteers. J Ultrasound 2022; 25(1): 59–65.
Wang B, Chen YY, Yang S, Chen ZW, Luo J, Cui XW et al. Combined Use of Shear Wave Elastography, Microvascular Doppler Ultrasound Technique, and BI-RADS for the Differentiation of Benign and Malignant Breast Masses. Front Oncol 2022; 12: 906501.
Liu H, Liao Q, Wang Y, Hu Y, Zhu Q, Wang L et al. A new tool for diagnosing parathyroid lesions: angio plus ultrasound imaging. J Thorac Dis 2019; 11(11): 4829–4834.
Freeman S, Bertolotto M, Richenberg J, Belfield J, Dogra V, Huang DY et al. Ultrasound evaluation of varicoceles: guidelines and recommendations of the European Society of Urogenital Radiology Scrotal and Penile Imaging Working Group (ESUR-SPIWG) for detection, classification, and grading. Eur Radiol 2020; 30(1): 11–25.
Kim HL, Chung J, Kim KJ, Kim HJ, Seo WW, Jeon KH et al. Lifestyle Modification in the Management of Metabolic Syndrome: Statement From Korean Society of CardioMetabolic Syndrome (KSCMS). Korean Circ J 2022; 52(2): 93–109.
Handelsman Y, Jellinger PS, Guerin CK, Bloomgarden ZT, Brinton EA, Budoff MJ et al. Consensus Statement by the American Association of Clinical Endocrinologists and American College of Endocrinology on the Management of Dyslipidemia and Prevention of Cardiovascular Disease Algorithm – 2020 Executive Summary. Endocr Pract 2020; 26(10): 1196–1224.
Barrett EJ, Liu Z, Khamaisi M, King GL, Klein R, Klein BEK et al. Diabetic Microvascular Disease: An Endocrine Society Scientific Statement. J Clin Endocrinol Metab 2017; 102(12): 4343–4410.
Sorop O, Olver TD, van de Wouw J, Heinonen I, van Duin RW, Duncker DJ et al. The microcirculation: a key player in obesity-associated cardiovascular disease. Cardiovasc Res 2017; 113(9): 1035–1045.
Houben A, Martens RJH, Stehouwer CDA. Assessing Microvascular Function in Humans from a Chronic Disease Perspective. J Am Soc Nephrol 2017; 28(12): 3461–3472.
Balasubramanian P, Kiss T, Tarantini S, Nyul-Toth A, Ahire C, Yabluchanskiy A et al. Obesity-induced cognitive impairment in older adults: a microvascular perspective. Am J Physiol Heart Circ Physiol 2021; 320(2): H740-H761.
Campbell DJ, Somaratne JB, Prior DL, Yii M, Kenny JF, Newcomb AE et al. Obesity is associated with lower coronary microvascular density. PLoS One 2013; 8(11): e81798.
Andreieva IO, Riznyk OI, Myrnyi SP, Surmylo NN. State of Cutaneous Microcirculation in Patients with Obesity. Wiadomości Lekarskie 2021; 74(9): 2039–2043.
Hernandez GN, Dabin C, del CGM, Rasia ML. Haemorheological variables in a rat model of hypertriglyceridaemic obesity and diabetes. Vet Res Commun 2002; 26(8): 625–35.
Vaya A, Hernandez-Mijares A, Bonet E, Sendra R, Sola E, Perez R et al. Association between hemorheological alterations and metabolic syndrome. Clin Hemorheol Microcirc 2011; 49(1–4): 493–503.
Kunadian V, Chieffo A, Camici PG, Berry C, Escaned J, Maas A et al. An EAPCI Expert Consensus Document on Ischaemia with Non-Obstructive Coronary Arteries in Collaboration with European Society of Cardiology Working Group on Coronary Pathophysiology & Microcirculation Endorsed by Coronary Vasomotor Disorders International Study Group. Eur Heart J 2020; 41(37): 3504–3520.
Mostafa T, Labib I, El-Khayat Y, El-Rahman El-Shahat A, Gadallah A. Human testicular arterial supply: gross anatomy, corrosion cast, and radiologic study. Fertil Steril 2008; 90(6): 2226–30.
Ergun S, Stingl J, Holstein AF. Segmental angioarchitecture of the testicular lobule in man. Andrologia 1994; 26(3): 143–50.

There is NO conflict of interest to disclose

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The role of testicular microcirculatory disorders in spermatogenic dysfunction in obese men

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Abstract

Figures

Introduction

Materials And Methods

Participant screening and enrollment

Instruments and Methods

Body mass index (BMI) calculation

Patient grouping according to BMI

Semen collection and analysis

Patient grouping according to semen results

Statistical analysis

Results

Participants screening and enrollment

Inter-observer agreement for UMVD

Age, sperm concentration, volume-mean, BMI and UMVD in different semen groups

Age, sperm concentration, Volume-mean and UMVD in different BMI subgroups

ROC curve of UMVD

Discussion

Declarations

References

Additional Declarations

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