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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 35  |  Issue : 2  |  Page : 762-768

Role of three-dimensional ultrasound and Doppler in differentiating leiomyoma and adenomyosis of uterus


1 Department of Obstetrics and Gynecology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Radiology, Faculty of Medicine, Menoufia University, Menoufia, Egypt

Date of Submission21-Oct-2021
Date of Decision29-Nov-2021
Date of Acceptance06-Dec-2021
Date of Web Publication27-Jul-2022

Correspondence Address:
Noha F Ahmed
Department of Obstetrics and Gynecology, Faculty of Medicine, Menoufia University, Shebin El-Kom, Menoufia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_214_21

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  Abstract 


Objective
The purpose of this study is to evaluate the importance of three-dimensional (3D) power Doppler ultrasound (US) in the diagnosis and differentiation of leiomyoma and adenomyosis of the uterus.
Background
The clinical presentation of adenomyosis and leiomyoma overlaps. The 3/4D US imaging has been currently able to produce female pelvis images that are comparable with magnetic resonance imaging and computerized tomography images in both quality and orientation, with the benefit of being without radiation and low cost.
Patients and methods
This study included female patients clinically diagnosed as having uterine leiomyoma and/or adenomyosis and were indicated for hysterectomy. By Doppler velocimetry with the use 3D power Doppler, the waveforms of the ascending main branch of the uterine artery were obtained on both sides of the cervix. Calculation of the resistance index (RI) and pulsatility index (PI) was done in an automatic manner. The averages of arteries on both sides were taken.
Results
The vascularity of most of the leiomyoma lesions was peripheral and of all of the adenomyosis lesions was central. The adenomyosis group showed significantly decreased vascular index, flow index, and vascular-flow index mean values (P < 0.01), significantly increased uterine artery RI mean values (P < 0.05), and highly significantly increased PI values (P < 0.01).
Conclusion
Three-dimensional US imaging with power Doppler can increase the accuracy of differentiation between leiomyoma and adenomyosis cases. Significant differences were noted in the vascularity site and Doppler indices.

Keywords: adenomyosis, leiomyoma, three-dimensional power Doppler ultrasound


How to cite this article:
El Aal NK, ELLakwa HE, Hassanein SA, Ahmed NF, Ammar HA. Role of three-dimensional ultrasound and Doppler in differentiating leiomyoma and adenomyosis of uterus. Menoufia Med J 2022;35:762-8

How to cite this URL:
El Aal NK, ELLakwa HE, Hassanein SA, Ahmed NF, Ammar HA. Role of three-dimensional ultrasound and Doppler in differentiating leiomyoma and adenomyosis of uterus. Menoufia Med J [serial online] 2022 [cited 2024 Mar 28];35:762-8. Available from: http://www.mmj.eg.net/text.asp?2022/35/2/762/352151




  Introduction Top


Adenomyosis is a benign uterine disorder characterized by the presence of endometrial tissue in an abnormal location within the myometrium. This process is associated with myometrial stroma hyperplasia or hy pertrophy[1]. Adenomyosis usually manifests in the age range from 40 to 50 years. Adenomyosis, being estrogen dependent, shows rapid regression after menopause. It remains a poorly understood disease[2]. As adenomyosis is often recorded according to the hospital reports, its actual incidence is still unknown. However, its incidence is generally estimated to range from 20% to 65%[2].

Leiomyoma (uterine fibroid) is the most common uterine benign neoplasm. Leiomyoma usually begins during the reproductive age period of females, as it has a hormone-responsive nature. Leiomyoma, as well as adenomyosis, regresses after menopause[3].

The clinical presentation of adenomyosis and leiomyoma overlaps. This yields considerable difficulty in differentiating both entities clinically. This differentiation is essential to follow a suitable management strategy for each disease[4].

Various imaging modalities have been considered in the differentiation between leiomyoma and adenomyosis with variable rates of success[5]. Of these modalities, the three-/four-dimensional ultrasound (3/4D US) imaging has been currently able to produce female pelvis images that are comparable with magnetic resonance imaging and computerized tomography images in both quality and orientation, with the benefit of being without radiation and low cost[4].

The 3D US imaging, with the use of power Doppler, has improved the objective reliable vascularity evaluation. Power Doppler US is highly sensitive, with less angle dependence and aliasing susceptibility when compared with color Doppler US. Power Doppler US is able to depict blood flow fluctuations, and it can be adopted for differentiation between leiomyoma and adenomyosis[6].

The purpose of this study is to evaluate the importance of the 3D power Doppler US in the diagnosis and differentiation of leiomyoma and adenomyosis of the uterus.


  Patients and methods Top


This is a descriptive cross-sectional study that was conducted in the departments of obstetrics and gynecology, radiology, and pathology of our university hospital during the period from March 2017 to March 2020. The study was commenced after the approval of research ethics committee. The sample size was calculated through Epi-info software (version 7). Based on previously reported 3D Doppler US test sensitivity and specificity for diagnosis of adenomyosis and leiomyoma, together with their prevalence, at confidence interval of 95% and precision 2%, a minimum of 117 cases should be included. To avoid cases dropout, this study included 157 patients.

This study included consecutive female patients, aged older than 40 years, who were admitted to the obstetrics and gynecology department over the study period, with clinical diagnosis of leiomyoma of uterus and/or adenomyosis, and were indicated for hysterectomy. Patients fit for conservative treatment, those who were pregnant, or those seeking for pregnancy were excluded from the study. Patients with huge fibroids or those having hormonal therapy before surgery were also excluded.

An informed written consent was obtained from each patient, and the study was conducted according to the Declaration of Helsinki.

Complete personal and obstetric history and comorbidities data were taken from each patient. Patients underwent dedicated clinical examination. The pelvic examination included vaginal and rectal bimanual examination, and per speculum examination.

Patients' US examination was performed using GE (General Electric Voluson E6®, manufactured by Medison-Kretz, Zipf, Korea-Austria) with a 3.5–5-MHz curvilinear probe for transabdominal US and TVS probe (6–9 9 Mhz). First, the patients were evaluated transabdominally with full bladder, then they were asked void urine, and a TVS was performed. All patients underwent examination with two-dimensional (2D) US examinations. The 3D power Doppler US was performed preoperatively as well. The adnexa and uterus were evaluated to exclude other gynecological pathologies.

Two-dimensional US was used for the assessment of the lesion site, size, echogenicity, and shape. In 3D power Doppler US examination, all quantitative measurements were performed by a single physician to obviate interobserver variability. The US evaluation was performed with the region of interest, including the lesion region in the uterus entirely. The examination included estimation of the lesion size and volume, assessment of the site of vascularity, and calculation of Doppler indices, that is, flow index (FI), vascular index (VI), and vascular-flow index (VFI) after adjustment of the Doppler settings. The virtual organ computer-aided analysis (VOCAL) software (Medison-Kretz, Zipf, Korea-Austria) was used for analyzing the 3D power Doppler histograms with computer algorithms to produce vascularization and blood flow indices.

Doppler US velocimetry of the uterine artery was performed with the use of 3D color Doppler, and the waveforms of the ascending main branch of the uterine artery were obtained on both sides of the cervix. Positioning of the Doppler was performed when identifying the vessel with appropriate color signals. Calculation of the resistance index (RI) and pulsatility index (PI) was obtained in an automatic manner when a proper wave was achieved. The averages of arteries on both sides were taken.

Patients underwent abdominal hysterectomy. Histopathological examination of lesions was performed by experienced pathologists, who were blind to the clinical and imaging findings.

The primary outcome measures in this study were the findings of 3D power Doppler US in cases of uterine leiomyoma and adenomyosis and the ability of this examination to differentiate between cases of uterine adenomyosis and leiomyoma.

Data management and analysis

Data were tabulated and introduced into a PC using Statistical Package for the Social Sciences (SPSS) version 22.0 (IBM, SPSS, Chicago, IL, USA). Descriptive analysis was performed: mean and SD values for numerical variables and frequency and percentage for categorical variables. Analytical statistics included analysis of variation test to obtain the difference between more than two groups, and Fisher's exact and χ2 tests for comparison of categorical data.

The result was considered as statistically nonsignificant if P value >0.05, statistically significant if P value ≤0.05, and statistically highly significant if P value ≤0.001.


  Results Top


In this study, the included 157 female patients had a mean age of 45.73 ± 3.93 years. The mean gravidity was 3.92 ± 1.48 and the mean parity was 3.25 ± 1.15 times. [Table 1] demonstrates the clinical presentation, the comorbidities, and the diagnostic data of the study patients. Every patient presented with one or more symptoms, with the most prevalent presentation being abnormal uterine bleeding (AUB), as it occurred in 87.9% of the patients, whereas 33.12% of the patients presented with chronic pelvic pain, and 10.19% presented with an abdominal lump. Regarding patient comorbidities, 3.8% of the patients had associated breast cancer, 23.57% had hypertension, and 25.48% had diabetes mellitus.
Table 1: Participants' demographic, clinical, and diagnostic data

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The mean uterine size in the study patients was 13.94 weeks. Most of the patients had intramural lesion (76.43%). Regarding lesion vascularity, the highest percentage was peripheral (59.23%). The most prevalent clinical and US diagnosis was leiomyoma (61.15%), whereas 31.21% of the patients had adenomyosis and 7.64% had combined lesions. Typically, the same diagnosis was found by the postoperative histopathological examination.

On classification of the study patients according to their final diagnosis, no significant differences were noted among the three groups of patients (leiomyoma, adenomyosis, and combined) concerning the mean age, gravidity, or parity (P > 0.05).

The differences among the three groups regarding the clinical and diagnostic data are illustrated in [Table 2]. There were no significant differences in the prevalence of chronic pelvic pain and AUB (P > 0.05). A highly significant difference was noted in the prevalence of lump presentation (P < 0.01), with no cases of the adenomyosis presented with lump. Regarding associated diseases, hypertension and breast cancer were found to be higher in the leiomyoma groups (either alone or with concomitant adenomyosis); this difference was significant in case of breast cancer (P = 0.03), yet it did not reach the level of significance in case of hypertension (P = 0.08). On the contrary, diabetes mellitus was found to be higher in the adenomyosis groups (either alone or with concomitant leiomyoma), with a statistically significant difference (P = 0.02).
Table 2: Comparison among the three groups (leiomyoma, adenomyosis, and combined) in the clinical and ultrasound findings

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There were highly significant differences among the three groups in the uterine size by weeks and site of the lesion (P < 0.01). The combined lesion group showed significantly increased mean value of the uterine size (21 + 1). Most of the patients in the leiomyoma and adenomyosis groups had the lesion intramural (71.88% and 100%, respectively), whereas the combined group showed a higher percentage of subserous lesion location (75%).

Regarding the site of lesion vascularity, it showed a highly significant difference among the studied groups (P < 0.01). The vascularity of most of the leiomyoma lesions was peripheral (93.75%), the vascularity of all of the adenomyosis lesions was scattered, and the vascularity of most of the combined lesions was difficult to assess (75%).

In the analysis of the 3D power Doppler findings, there were highly significant differences among the groups. The adenomyosis group showed a highly significant decrease in VI, FI, and VFI mean values (P < 0.01), a significant increase in uterine artery RI mean values (P < 0.05), and a highly significant increase in PI values (P < 0.01).

Conducting receiver operating characteristic curves analysis for the use of the 3D power Doppler parameters in differentiation between leiomyoma and adenomyosis revealed that the best indicators were VI, FI, and VFI, with areas under the curve (AUC) of 99.7%, 99.7%, and 99.8%, respectively. For VI, the cutoff value was 0.9, with a sensitivity of 100% and a specificity of 88.5%. FI cutoff value was 42.39, with a sensitivity of 100% and a specificity of 88.5%, and VFI cutoff value was 0.48, with a sensitivity of 100% and a specificity of 93.7%. The uterine artery RI and PI showed weak differentiation power (AUC <50%) [Figure 1].
Figure 1: ROC curve for assessment of the 3D power Doppler parameters in differentiation between leiomyoma and adenomyosis.

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[Image 1]a, [Image 1]b and [Image 2]a, [Image 2]b present VOCALTM in a case of adenomyosis and a case of leiomyoma.




  Discussion Top


AUB is a prevalent manifestation of gynecologic disease, particularly premenopausal. Adenomyosis and leiomyoma are the two mainly encountered causes of AUB[4]. Both disorders affect females during their reproductive age and regress after menopause. Differentiating between them is critically essential to take a proper treatment decision[5].

US is a simple imaging method, which has the advantages of being noninvasive, not eliciting radiation, and of relatively low cost. 3D US facilitates obtaining a volume-based real image from 2D images[7]. 3D US acquits an anatomic volume, which includes the entire needed data, rather than just a slice. From the stored volume information, any view shows the ability to be reformatted and analyzed[8].

The purpose of this study is to evaluate the importance of the 3D power Doppler US in the diagnosis and differentiation of leiomyoma and adenomyosis of the uterus. This study included 157 patients who had a clinical diagnosis of leiomyoma and/or adenomyosis and indicated for hysterectomy.

In this study, the most prevalent clinical and US diagnosis was leiomyoma (61.15%), whereas 31.21% of the patients had adenomyosis and 7.64% had combined lesions. Typically, the same diagnosis was found by the postoperative histopathological examination. These percentages were found comparable with those reported by the study by Sharma et al.[4]. They investigated 96 Indian females diagnosed clinically as having leiomyoma and/or adenomyosis. They reported that the percentage of leiomyoma cases was 60%, the percentage of adenomyosis cases was 31%, and that of both conditions was 8%. This was the final diagnosis. However, their preliminary clinical diagnosis failed to diagnose the cases that had both conditions in their study.

The coexistence of leiomyoma and adenomyosis was previously reported. Taran et al. reported this coexistence, but with a higher incidence; it was between 15% and 57% in their study[9].

The mean age of the study patients was 45.73 years, the mean gravidity was 3.92, and the mean parity was 3.25 times. No significant differences were noted among the three groups (leiomyoma, adenomyosis, and combined) regarding the mean age, gravidity, or parity.

The most prevalent presentation in this study's patients was AUB (87.9%), followed by chronic pelvic pain (33.12%) and lump (10.19%). No significant differences were noted among the three groups of patients in the prevalence of chronic pelvic pain and AUB (P > 0.05). A highly significant difference was noted in the prevalence of lump presentation (P < 0.01), with no cases of the adenomyosis presented with lump.

Our findings agree with multiple previous studies that indicated AUB as the most common presentation of uterine fibroids [10–12], and adenomyosis[13]. The findings of this study align with Elkattan et al.[5] and Sharma et al.[4], as they reported AUB as the most prevalent symptom in their studies populations, with no significant difference among groups. However, in contradiction to the aforementioned studies, the study by Krentel and DeWilde reported that dysmenorrhea is the most common presentation in patients with adenomyosis[14].

Regarding the associated diseases, in this study, hypertension and breast cancer were found to be higher in the leiomyoma groups (either alone or with concomitant adenomyosis). This difference was significant in case of breast cancer (P = 0.03), yet it did not reach the level of significance in case of hypertension (P = 0.08). On the contrary, diabetes mellitus was found to be higher in the adenomyosis groups (either alone or with concomitant leiomyoma), with a statistically significant difference (P = 0.02).

In harmony with our study, a significant association between diabetes mellitus and adenomyosis was also reported recently[15]. This may be explained by their sharing common hormonal, genetic, and autoimmune pathways or obesity as a risk factor for both. The association between hypertension and uterine leiomyoma was found in various types of studies [16–19]. Faerstein et al.[17] suggested hypertension as a proatherogenic state that enhances the development of fibroid in the same manner of developing atherosclerotic alterations in the smooth muscle of the arterial wall. This was supported by a more recent systematic review conducted by Haan et al.[20], concluding an association between uterine fibroids and hypertension.

There is controversy about the association between uterine leiomyoma and the breast cancer risk. Two recent studies supported this association[21],[22]. Of them, Shen et al.[22] in 2017 concluded that despite this association, the breast cancer overall mortality was lower in patients with leiomyoma. On the contrary, a large-scale study denied this association[23].

Most of the patients in the leiomyoma and adenomyosis groups had the lesion intramural, whereas the combined group showed a higher percentage of subserous lesion location. The prevalence of intramural type of leiomyoma is well documented. Intramural myomas are the most prevalent of all the leiomyomas[24].

Regarding the site of lesion vascularity, a highly significant difference among the studied groups was noted. The vascularity of most of the leiomyoma lesions was peripheral, for all of the adenomyosis lesions was scattered, and for most of the combined lesions was difficult to assess.

In this respect, some previous studies showed congruent studies. In their study, Exacoustos et al.[25] reported that adenomyosis showed diffuse vessels, whereas leiomyoma showed peripheral vascularity with a ring appearance. Moreover, the study by Sharma et al. reported that adenomyosis mostly showed central or diffuse vascularity, whereas leiomyoma mostly showed peripheral vascularity in 89% cases of fibroid. Our findings were in agreement also with those of El Kattan et al. and Cheng et al., who documented that peripheral vascularity was mostly shown in leiomyoma, whereas scattered vascularity was mostly shown in adenomyosis[5],[6].

In the analysis of the 3D power Doppler findings, there was a highly significant difference among the groups. The adenomyosis group showed highly significantly decreased VI, FI, and VFI mean values (P < 0.01), significantly increased uterine artery RI mean values (P < 0.05), and highly significantly increased PI values (P < 0.01).

In similarity with this study, the study of Sharma et al.[4] found that in leiomyoma, they reported higher velocity flow in leiomyoma cases than in adenomyosis cases.

In consistency with this study, the studies of Elkattan et al. and Cheng et al. also showed that 3D power Doppler indices were significantly higher in leiomyoma cases[5],[6]. Moreover, in the study by Cheng et al.[6], the authors reported mean values that were comparable with ours. Minsart et al.[26] also found a statistical difference in the 3D power Doppler indices between the cases of leiomyoma and adenomyosis.

However, the results of Elkattan et al.[5] were not in discordance with ours regarding the indices of the uterine artery (RI and PI). They found a nonsignificant difference between the leiomyoma and adenomyosis in the indices of uterine artery.


  Conclusion Top


Three-dimensional US imaging with power Doppler can increase the accuracy of differentiation between leiomyoma and adenomyosis cases. Significant differences were noted in the vascularity site and Doppler indices.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Dessouky R, Gamil S, Nada MG. Management of uterine adenomyosis: current trends and uterine artery embolization as a potential alternative to hysterectomy. Insights Imaging 2019; 10:48.  Back to cited text no. 1
    
2.
Upson K, Missmer SA. Epidemiology of adenomyosis. Semin Reprod Med 2020; 38:89-107.  Back to cited text no. 2
    
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Giuliani E, As-Sanie S, Marsh EE. Epidemiology and management of uterine fibroids. Int J Gynaecol Obstet 2020; 149:3-9.  Back to cited text no. 3
    
4.
Sharma K, Bora MK, Venkatesh BP. Role of 3D ultrasound and Doppler in differentiating clinically suspected cases of leiomyoma and adenomyosis of uterus. J Clin Diagn Res 2015; 9:QC08-QC12.  Back to cited text no. 4
    
5.
Elkattan E, Kamel R, Elghazaly H, ElAriki E. Can three-dimensional (3D) power Doppler and uterine artery Doppler differentiate between fibroids and adenomyomas? Middle East Fertil Soc J 2016; 21:46-52.  Back to cited text no. 5
    
6.
Cheng Y, Chen Y, Hsu Y, Cheng Y, Chen M, Hsu Y. Preoperative three-dimensional power Doppler ultrasonographic evaluation of adenomyosis and uterine leiomyoma. Dig J Nanomater Bios 2012; 7:621-627.  Back to cited text no. 6
    
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Huang Q, Zeng Z. A review on real-time 3D ultrasound imaging technology. Biomed Res Int 2017; 17:602-609.  Back to cited text no. 7
    
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Saleh A, Al-Saygh F, Abushama M, Ahmed B. The role of three-dimensional ultrasound in gynecology. Res Womens Health 2019; 1:4-11.  Back to cited text no. 8
    
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Taran FA, Stewart EA, Brucker S. Adenomyosis: epidemiology, risk factors, clinical phenotype and surgical and interventional alternatives to hysterectomy. Geburtshilfe Frauenheilkd 2013; 73:924–931.  Back to cited text no. 9
    
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Shaheen S, Naheed T, Sadaf F, Rahim R. Menorrhagia due to fibroids and its management. JSOGP. 2013; 3:231-235.  Back to cited text no. 10
    
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Munusamy MM, Sheelaa WG, Lakshmi VP. Clinical presentation and prevalence of uterine fibroids: a 3-year study in 3-decade rural South Indian women. Int J Reprod Contracept Obstet Gynecol 2017; 6:5596-5601.  Back to cited text no. 11
    
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Khyade RL. A study of menstrual disturbance in cases of fibroid uterus. Int J Reprod Contracept Obstet Gynecol 2017; 6:2494-2497.  Back to cited text no. 12
    
13.
Donato N, Seracchioli R. How to evaluate adenomyosis in patients affected by endometriosis? Minim Invasive Surg 2014; 20:17.  Back to cited text no. 13
    
14.
Krentel H, DeWilde RL. How to diagnose and treat adenomyosis in patients with endometriosis. J Rep Med Endocr 2018; 15:262-269.  Back to cited text no. 14
    
15.
Yeh CC, Su FH, Tzeng CR, Muo CH, Wang WC. Women with adenomyosis are at higher risks of endometrial and thyroid cancers: a population-based historical cohort study. PLoS One. 2018; 13:e0194011.  Back to cited text no. 15
    
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Luoto R, Rutanen E, Auvinen A. Fibroids and hypertension: a cross-sectional study of women undergoing hysterectomy. J Reprod Med 2001; 46:359–364.  Back to cited text no. 16
    
17.
Faerstein E, Szklo M, Rosenshein NB. Risk factors for uterine leiomyoma: a practice-based case-control study. II. Atherogenic risk factors and potential sources of uterine irritation. Am J Epidemiol. 2001; 153:11–19.  Back to cited text no. 17
    
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Boynton-Jarrett R, Rich-Edwards J, Malspeis S, Missmer SA, Wright R. A prospective study of hypertension and risk of uterine leiomyomata. Am J Epidemiol 2005; 161:628-638.  Back to cited text no. 18
    
19.
Aboyeji AP, Ijaiya MA. Uterine fibroids: a ten-year clinical review in Ilorin, Nigeria. Niger J Med 2002; 11:16–19.  Back to cited text no. 19
    
20.
Haan Y, De Lange M, Suhooli H, Ankum W, Timmermans T, Limpens J, et al. The association between hypertension and uterine fibroids: a systematic review and meta-analysis. J Hypert. 2015; 33:117-125.  Back to cited text no. 20
    
21.
Chuang SC, Wu GJ, Lu YS, Lin CH, Hsiung CA. Associations between medical conditions and breast cancer risk in Asians: a nationwide population-based study in Taiwan. PLoS One. 2015; 10:e0143410.  Back to cited text no. 21
    
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Shen TC, Hsia TC, Hsiao CL, Lin CL, Yang CY, Soh KS, et al. Patients with uterine leiomyoma exhibit a high incidence but low mortality rate for breast cancer. Oncotarget 2017; 8:33014.  Back to cited text no. 22
    
23.
Wise LA, Sponholtz TR, Rosenberg L, Adams-Campbell LL, Kuohung W, LaValley MP, et al. History of uterine leiomyoma and risk of endometrial cancer in black women. Cancer Causes Control 2016; 27:545–552.  Back to cited text no. 23
    
24.
Thompson M, Carr B. Intramural myomas: to treat or not to treat. Int J Womens Health 2016; 8:145-149.  Back to cited text no. 24
    
25.
Exacoustos C, Luciano D, Corbett B, De Felice G, Di Feliciantonio M, Luciano A, et al. The uterine junctional zone: a 3-dimensional ultrasound study of patients with endometriosis. Am J Obstet Gynecol 2013; 209:248.e1–248.e7.  Back to cited text no. 25
    
26.
Minsart AF, Ntoutoume Sima F, Vandenhoute K, Jani J, Van Pachterbeke C. Does three-dimensional power Doppler ultrasound predict histopathological findings of uterine fibroids? A preliminary study. Ultrasound Obstet Gynecol 2012; 40:714-720.  Back to cited text no. 26
    


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