Prediction of nonmass breast cancer based on ultrasound and molybdenum target characteristics

doi:10.21203/rs.3.rs-3230407/v1

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Prediction of nonmass breast cancer based on ultrasound and molybdenum target characteristics

https://doi.org/10.21203/rs.3.rs-3230407/v1

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To investigate the effect of ultrasound and molybdenum target X-ray characteristics in predicting nonmass breast cancer. We retrospectively analyzed the data of 185 nonmass breast lesion patients between September 2019 and 2021. Benign and malignant nonmass breast lesions were typed into lamellar hypoechoic, ductal alteration, microcalcification, and structural disorder types, as seen on ultrasonography. In addition, the differences in molybdenum target X-ray parameters, ultrasonographic manifestations and ultrasound characteristics among individuals with nonmass breast lesions were studied. Ultrasound manifestation of microcalcified type and suspicious malignancy on molybdenum target X-ray evaluation were independently associated with nonmass breast cancer and the difference was statistically significant (p<0.05). The subsequent logistic regression model was as follows: Logit (P) =-1.757+2.194microcalcification type on ultrasound + 1.520suspicious malignancy on molybdenum target X-ray evaluation. The areas under the ROC curves for microcalcification type on ultrasound, suspicious malignancy on molybdenum target X-ray, and the diagnostic model were 0.733, 0.667, and 0.827, respectively.Using ultrasound and molybdenum targets for diagnosis can increase the accuracy in finding nonmass breast cancer.The findings of this study can help improve the rate of detecting nonlumpy breast cancer and provide an imaging basis for improving the prognosis of breast cancer patients.

Biological sciences/Cancer

Health sciences/Diseases

Health sciences/Medical research

Health sciences/Oncology

Health sciences/Risk factors

nonmass type

ultrasonographic manifestations

molybdenum target X-ray

logistic regression

correlation

Breast illnesses are widespread and heterogenous diseases in women, and their incidence and malignancy rates are gradually increasing¹. In addition, patients with breast diseases tend to be younger. Therefore, it is important to address ways to improve the prognosis and quality of life of breast cancer patients and to increase the detection rate and diagnostic compliance rate for early breast cancer. Breast cancer has a variable presentation on ultrasound, with the mass type being the most prevalent^2–4. However, some breast cancer ultrasonograms lack conventional mass characteristics, and thus the lesions have a nonmass-type presentation with hazy boundaries and no discernible spatial occupancy impact in two separate vertical views⁵.According to the fifth ACR BI-RADS guideline⁶, structural disorders, ductal alterations, and other breast ultrasound-related signs may be the only ultrasound characteristics of nonmass breast cancer^7,8. However, ultrasound images that demonstrate these signs are not easily recognizable, frequently challenging to recognize correctly and have low diagnostic sensitivity, which can result in a missed diagnosis and a misdiagnosis^9–11.Therefore, their ultrasonographic manifestations are still challenging to recognize clinically. To increase the ultrasound diagnostic conformity rate of nonmass breast cancer and provide an imaging basis for identifying the lesions, we compared the clinical, ultrasound and mammography features of malignant nonmass breast cancer and compared them with those of benign nonmass breast lesions.

General information

The patients were enrolled from September 2019 to September 2021 at a hospital. The clinical data of 185 female patients (aged 24–76 (54.23 ± 10.82) years) with nonlumpy breast lesions confirmed by surgical or puncture biopsy pathology were collected.

Instrument and inspection method

The ultrasound examination was performed with GE Logiq E9 and French Acoustics Aixplorer color Doppler ultrasound diagnostic instruments with a frequency of 7–12 MHz; the mammography examination was performed with a fully digital mammography machine, model Selenia Dimensions (SDM-05000-2DC), manufactured by Hologic, USA, with the instrument in fully automatic exposure mode.

Basic clinical data (age, family history, the age of menarche, whether the patient in menopause, etc.) and the medical history of the subject were thoroughly gathered before the assessment. The subject was positioned supine, with both breasts and axillae fully exposed. Nipple discharge was checked, and the subject's breasts were bilaterally palpated.

Ultrasound: The nipple was used as the center of a two-dimensional grayscale ultrasound scan spanning from the external superior quadrant and proceeding in a radial pattern to the external inferior, internal inferior, and internal superior mammary glands as well as the nipple and areola regions. The bilateral mammary glands were scanned for comparison and examined for lamellar hypoechogenicity, ductal alterations, microcalcifications and structural disorders in glandular tissue. When a lesion was discovered, the best display view was chosen, and the position of the lesion was noted, utilizing the zoom key if necessary. The lesion's ultrasound characteristics were assessed, including posterior echogenicity and the presence of abnormal axillary lymph nodes (considered if any of the following conditions was met: aspect ratio 2, lymph node cortical thickness > 4 mm or asymmetric thickening, loss of portal structures, nonportal blood flow such as central, peripheral, or mixed, liquefied areas visible within, and visible calcified foci)¹². Then, we switched to color Doppler mode and adjusted the sampling frame size, color gain level and flow rate scale to obtain the best Doppler image of the lesion.

Molybdenum target X-ray: The subject was placed in a standing position with the chest fully exposed. Then, the breast was placed between the X-ray table and the compression device and sequentially photographed in the cephalocaudal and internal and external oblique positions in the fully automated exposure mode, with local compression and magnification if necessary. The photographs were automatically uploaded to the workstation for postprocessing.

Image analysis

The images (ultrasound and molybdenum target X-ray) of all lesions were jointly reviewed by two ultrasound physicians and radiologists with over 10 years of experience, who classified the nonmass breast lesions as either benign or malignant. The ultrasound physicians and radiologists both used a double-blind method to analyze the images, ignoring the pathological results of the subjects before making the final diagnosis.

Ultrasound image analysis: Combining the current classification methods^2,5,13,14 and the types of cases in this study, nonmass breast lesions were summarized into four types according to their ultrasound findings: ① lamellar hypoechoic type: a lesion with different echogenicity from the surrounding adjacent glandular tissue or the gland in the same area of the other side of the breast, limited asymmetry without clear borders and without clear occupancy on multisection sweep ② ductal alteration type: limited ductal widening and dilatation parallel to the ductal direction or isolated solid nodules within the ducts, uneven changes in ductal wall thickness and variable luminal diameter; ③ microcalcification type: dotted, linear or clustered microcalcifications within the lamellar hypoechoic area or the ductal hypoechoic lesions, or microcalcifications as the only sign of the lesion; ④ structural disorder type: tangled and distorted glandular structures in the lesion area, with unclear layers, uneven echogenic changes and blurred borders.

Molybdenum target X-ray image analysis: The normalized terminology of molybdenum target X-ray provided by the ACR BI-RADS 5th edition was used to classify the breast glands into four types: adipose, scattered glandular, non-uniform glandular and dense glandular. There are four types of molybdenum target X-ray signs: negative, calcified, distorted or asymmetrical, distorted or asymmetrical with calcification, and unilateral ductal dilatation. In this study, the results of molybdenum target X-ray evaluation were divided into two groups: negative and suspicious for malignancy. Category 1, 2 or 3 were assessed as negative for malignancy and category 0, 4 or 5 were assessed as suspicious for malignancy according to the BI-RADS.

Statistical analysis

SPSS 25.0 software was used for statistical analysis. Measurement data were tested for distribution normality and are expressed as the mean ± standard deviation (x ± s) if they conformed to a normal distribution, and the t test for independent samples was used for comparisons between the two groups. The chi-square test or Fisher's exact test was employed. Counting data are reported as instances or rates (%). Multifactorial analysis was performed using binary multifactorial logistic regression analysis. Factors closely associated with the diagnosis of nonmass breast cancer were screened to establish a binary logistic regression model to determine the best predictive characteristics. Receiver operating characteristic (ROC) curves were plotted, and the area under the curve (AUC) was calculated. A difference was considered statistically significant at P < 0.05.

Pathology results

Among the 185 nonmass breast lesions collected in this study, 100 were benign and 85 were malignant. The malignant group included 36 cases of ductal carcinoma in situ (42.4%), 29 cases of invasive ductal carcinoma (34.1%), 5 cases of invasive lobular carcinoma (6.9%), and 15 cases of ductal carcinoma in situ combined with invasive ductal carcinoma (17.6%).

Ultrasonographic manifestation typing

The lamellar hypoechoic type (71/185, 38.4%) was the most prevalent ultrasonographic manifestation among the 185 nonmass breast lesions, followed by the microcalcification type (56/185, 30.3%), ductal alteration type (36/185, 19.4%), and structural disorder type (22/185, 11.9%) (Fig. 1). The difference in the proportion of microcalcification type between the benign and malignant group was statistically significant (P < 0.05) (Table 1).

		Benign n (%)	Malignant n (%)	Total n (%)	χ²	P value
					9.138	0.028*
ultrasonographic manifestation	Lamellar hypoechoic type	42 (42.0)	29 (34.1)	71 (38.4)	1.207	0.272
	Ductal alteration type	23 (23.0)	13 (15.3)	36 (19.4)	1.741	0.187
	Microcalcification type	21 (21.0)	35(41.2)	56 (30.3)	8.861	0.003*
	Structural disorder type	14(14.0)	8(9.4)	22(11.9)	0.923	0.337
*mean P < 0.05;

Table 1. Comparison of ultrasonographic manifestations of patients with nonmass breast lesions (benign and malignant groups)

Ultrasound characteristics

The characteristics of the posterior echogenicity among nonmass breast lesions did not statistically differ between the benign and malignant groups (all P > 0.05); however, there was a statistically significant difference between the two groups regarding the presence of abnormal axillary lymph nodes and the grade of the blood flow signal (all P < 0.05). (In Table 2)

		Benign n (%)	Malignant n (%)	Total n (%)	χ²	P value
Posterior echo	No change	40 (40.0)	37 (43.5)	77 (41.6)
	Enhancement	32 (32.0)	18 (21.2)	50 (27.0)	2.909	0.234
	Attenuation	28 (28.0)	30 (35.3)	58 (31.4)
Lymph nodes	Abnormal	23 (23.0)	37 (43.5)	60 (32.4)	8.837	0.003^*
Lymph nodes	Normal	77 (77.0)	48 (56.5)	125 (67.6)	8.837	0.003^*
Blood signal classification	Class 0/1	59 (59.0)	33 (38.8)	92 (49.7)	7.482	0.006^*
Blood signal classification	Class 2/3	41 (41.0)	52 (61.2)	93 (50.3)	7.482	0.006^*
* mean P < 0.05

Table 2. Comparison of ultrasound characteristics of patients with nonmass breast lesions (benign or malignant group)

Molybdenum target X-ray parameters

There was no statistically significant difference between the benign group and the malignant group in terms of breast gland type (P > 0.05); among the molybdenum target X-ray signs, there was no statistically significant difference between the benign group and the malignant group in terms of negative, calcified, structurally distorted or asymmetric, and unilateral ductal dilatation types (all P > 0.05). However, the difference between the benign group and the malignant group in terms of distorted or asymmetrical structure with calcification type was statistically significant (P < 0.05). When molybdenum target X-ray was used to evaluate suspicious malignancy, the pathological result was significantly more likely to be malignant (P < 0.05) (Table 3 and Fig. 2).

		Benign n (%)	Malignant n (%)	Total n (%)	t/χ²	P value
Molybdenum target X-ray gland type	Fatty type	21(21.0)	11(12.9)	32(17.3)	3.069	0.387
	Scattered glandular type	27(27.0)	31(36.5)	58(31.4)
	Heterogeneous glandular type	20(20.0)	17(20.0)	37(20.0)
	Dense glandular type	32(32.0)	26(30.6)	58(31.4)
					14.832	0.004^*
	-	32(32.0)	17(20.0)	49(26.5)	3.398	0.065
	Calcified	40(40.0)	23(27.1)	63(34.1)	3.426	0.064
	Distorted or asymmetrical structure	15(15.0)	18(21.2)	33 (17.8)	1.196	0.274
	Distorted or asymmetrical structure with calcification	12(12.0)	24(28.2)	36 (19.4)	7.727	0.005^*
	Unilateral ductal dilatation	1(1.0%)	3(3.5%)	4 (2.2%)	0.045	0.502
Molybdenum target X-ray evaluation	No suspicious malignancy	76 (76.0%)	18 (21.2%)	94 (50.8%)	55253	< 0.001*
Molybdenum target X-ray evaluation	Suspicious malignancy	24 (24.0%)	67 (78.8%)	91 (49.2%)	55253	< 0.001*
* mean P < 0.05

Table 3. Comparison of molybdenum target X-ray parameters of patients with nonmass breast lesions (benign and malignant groups)

Multifactor logistic regression analysis

Multifactor logistic regression analysis showed that the ultrasonographic manifestation of microcalcification type and the molybdenum target X-ray assessment of suspicious malignancy were independently and significantly associated with a diagnosis of nonmass breast cancer (B 2.194 and 1.520, respectively; both P < 0.05) (see Table 4). A multifactorial logistic regression model was established as follows: Logit (P)= -1.757 + 2.194*ultrasonographic manifestation of microcalcification type·+1.520*molybdenum (Mg) target X-ray assessment of suspicious malignancy. Using the pathological findings as the gold standard, the model yielded a correct rate of 69.7% (Table 5). The areas under the ROC curve for the ultrasonographic manifestation of microcalcification type, the molybdenum target X-ray assessment of suspicious malignancy and the diagnostic model were 0.733, 0.667 and 0.827, respectively (Fig. 3).

factor	B	SE	χ²	P	OR	95% confidence interval
factor	B	SE	χ²	P	OR	Upper bound	Lower bound
Axillary lymph nodes (normal or abnormal)	1.150	0.799	2.070	0.150	3.159	0.659	15.138
Blood signal	0.423	0.677	0.391	0.532	1527	0.405	5.761
Ultrasonographic manifestation: microcalcification type	2.194	0.710	9.555	0.002^*	8.973	2.232	36.073
Molybdenum target X-ray sign: Distorted or asymmetrical structure with calcification	0.468	0.745	0.394	0.530	1.597	0.370	6.882
Molybdenum target X-ray evaluation: Suspicious malignancy	1.520	0.706	4.628	0.031^*	4.571	1.145	18.252
Constant	-1.757	0.589	8.893	0.003^*	0.173

^*mean P<0.05

Table 4. Multivariate logistic regression analysis of factors influencing nonmass breast cancer

		Pathology result of nonmass breast lesions
		Benign lesions (n)	Malignant lesions (n)
Prediction result	Benign lesion	69	25
	Malignant lesion	31	60
Prediction accuracy		69.7%

Table 5. Logistic regression model prediction

The results of this study showed that nonmass breast lesions were significantly more likely to be malignant (P < 0.05) if they presented with the ultrasonographic findings of abnormal axillary lymph nodes, abundant lesion blood flow signal, and the microcalcification type; the molybdenum target X-ray sign of distorted or asymmetrical structure with calcification type; and the molybdenum target X-ray evaluation of suspicious malignancy, in agreement with the findings of Ko et al¹⁵.

An important characteristic that can differentiate between benign and malignant nonmass breast lesions is the involvement of the axillary lymph nodes^16,17. Because invasion of the axillary lymph nodes by tumor cells means, to a certain extent, that the breast cancer has advanced to the middle and advanced stages, the possibility of malignant lesions should be considered when nonlumpy breast cancer lesions are accompanied by abnormal axillary lymph nodes^5,18. However, the number of patients in this study with abnormal axillary lymph nodes among those with malignant lesions was 37 (43%), which is insufficient to prove definitively that abnormal axillary lymph nodes are an indicator of nonmass breast cancer. In addition, it has been noted that there is considerable overlap between the ultrasound imaging of some benign, hyperplastic, enlarged lymph nodes and those of metastatic, abnormal axillary lymph nodes. Therefore, there are limitations in determining the benignity and malignancy of nonmass breast lesions based only on axillary lymph node abnormalities¹⁹. XXX

Nonmass breast cancer tumor cells secrete angiogenic factors, and the subsequent neovascularization is responsible for tumor cell growth and proliferation²⁰. Choi et al. found that high vascular density was linked to malignant nonmass breast lesions²¹, whereas low vascular density was linked to benign nonmass breast lesions. In the current study, significantly more malignant nonmass breast lesions (61.2%) had blood flow signals classified as grade 2/3 than benign lesions (41.0%; P < 0.05), indicating that malignant nonmass breast lesions had a higher blood flow signal than benign lesions, in line with Zhang et al.²².

The ultrasound results of this study found that among the various ultrasonographic manifestations of nonmass breast lesions, the malignant group was significantly more likely to present with the ultrasonographic manifestation of the microcalcification type than the benign group (P < 0.05), indicating that microcalcified breast lesions can provide a meaningful evidence for the detection of non-lumpy breast cancer, which is consistent with the findings of Kim et al.²³. And Keränen et al.²⁴ found that ultrasound had a higher detection rate for microcalcified nonmass breast malignant lesions than benign lesions. The lack of nutrients in nonmass breast cancer lesions leads to massive tumor cell necrosis and lysis. An increase in calcium ions leads to calcium salt deposition and calcification foci²⁵. Microcalcifications are an important indication of nonmass breast cancer^26,27 and may even be the only ultrasound characteristic of malignant nonmass breast lesions²⁸. Kim et al.²³ reported that detecting microcalcifications on molybdenum target X-ray in nonmass breast lesions improved the accuracy of the differential diagnosis of nonmass breast lesions.

The molybdenum target X-ray results of this study confirmed the hypothesis of Kim et al., showing that molybdenum target X-ray characteristics play a guiding role in the differential diagnosis of nonmass breast lesions by showing that significantly fewer patients in the benign group presented with the molybdenum target X-ray sign of distorted or asymmetrical structures with calcification and the molybdenum target X-ray evaluation of suspicious malignancy than the malignant group (P < 0.05)²³. An important reference for diagnosing nonmass breast cancer is Ko et al.¹⁵, who found that the molybdenum target X-ray evaluation of suspected malignancy was substantially connected with nonmass breast cancer.

The present study included different ultrasound types of nonmass breast lesions in a multifactorial logistic regression analysis. The results showed that the ultrasonographic manifestation of microcalcification type was an independent risk factor for nonmass breast cancer^29,30, while this kind of perspective was ignored in the research of Ko et al. The results of the multifactorial logistic regression^31–33 analysis in this study also showed that whether the axillary lymph nodes were abnormal, blood flow signal grade, and the molybdenum target X-ray sign of structural distortion or asymmetry with calcification, which were statistically significant in the univariate analysis, were not significant in the regression analysis, while the molybdenum target X-ray evaluation of suspicious malignancy and the ultrasonographic manifestation of microcalcifications were identified as risk factors for nonmass breast cancer.

The areas under the ROC curves for ultrasonographic manifestation microcalcification type, molybdenum target X-ray suspicious malignancy, and diagnostic model, according to the regression model created in this study, were 0.733, 0.667, and 0.827, respectively, showing that the model has better diagnostic efficacy than the single factors. Studies from other countries have shown that segmental or aggregated calcifications, microcalcifications inside dilated ducts, and microcalcifications within hypoechoic zones are all easily detected on ultrasonography and indicate a greater risk of malignancy²³. When suspected malignant lesions are found on molybdenum target X-ray and microcalcification-type nonmass breast lesions are seen on ultrasound, a high suspicion of malignant lesions should be raised, and the patient should be monitored carefully.

The present study has some limitations: (i) The sample size of this study is too small and does not include uncommon nonmass breast cancer types such as breast lymphoma and breast mucinous carcinoma. Such cases should be studied further by increasing the number of samples; (ii) only one molybdenum target X-ray imaging result is included in this study; however, in the future, this result will be combined with MRI and other ultrasound techniques for in-depth comparative study.

In conclusion, there are differences between benign nonmass breast lesions and nonmass breast cancer in terms of ultrasound characteristics (abnormal axillary lymph nodes, blood flow signal grade, and microcalcifications) and molybdenum target X-ray characteristics (distorted or asymmetrical structures with calcifications and suspicious malignancy on molybdenum target X-ray). Therefore, the accuracy in diagnosing nonmass breast cancer could be increased using ultrasound and molybdenum target X-ray together. However, the study's sample size was small, so additional studies with larger sample sizes are needed.

Data availability

The datasets generated and/or analysed during the current study are not publicly available due protect patient privacy but are available from the corresponding author on reasonable request.

Statement

All methods were carried out in accordance with relevant guidelines and regulations in this paper. All experimental protocols were approved by the ethics committee/IRB of First Hospital of Shanxi Medical University and the informed consent was obtained from all subjects and/or their legal guardian(s).

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No competing interests reported.

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Prediction of nonmass breast cancer based on ultrasound and molybdenum target characteristics

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Abstract

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Introduction

Information and methods

General information

Instrument and inspection method

Image analysis

Statistical analysis

Result

Pathology results

Ultrasonographic manifestation typing

Ultrasound characteristics

Molybdenum target X-ray parameters

Multifactor logistic regression analysis

Discussion

Declarations

References

Additional Declarations

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