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Journal of X-Ray Science and Technology xx (20xx) x–xx

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DOI 10.3233/XST-18388
IOS Press

1 Performance evaluation of breast


2 cancer diagnosis with mammography,

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ultrasonography and magnetic resonance

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4 imaging

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5 Hang Suna , Hong Lia,∗ , Shuang Sia , Shouliang Qia , Wei Zhanga , He Maa , Siqi Liua ,
6 Yingxue Lia and Wei Qiana,b
a
7 Sino-Dutch Biomedical and Information Engineering School, Northeastern University,

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8 Shenyang, Liaoning, China
b
Department of Electrical and Computer Engineering, University of Texas, El Paso, TX, USA

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10 Received 12 March 2018
11 Revised 1 July 2018
12 Accepted 16 July 2018

13 Abstract.
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14 OBJECTIVE: Various imaging modalities have been used to diagnose suspicious breast lesions. Purpose of this study is to
15 compare the diagnostic accuracy for breast cancer using mammography, ultrasonography and magnetic resonance imaging
(MRI).
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17 METHODS: Total 107 patients aged from 19 to 62 years are included in this retrospective study. Mammography, ultrasonog-
18 raphy and MRI scans were performed for each patient detected with suspected breast tumor within a month. In addition, the
19 tumor diversity (10 types of benign and 5 types of malignant) was confirmed by pathological findings of tumor biopsy. To
20 compare the diagnosis performance of the three imaging modalities, the overall fraction correct (accuracy), positive predict
21 value (PPV), negative predict value (NPV), sensitivity and specificity were calculated. Meanwhile, the receiver operating
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22 characteristic (ROC) analysis was also performed.


23 RESULTS: The diagnostic accuracy ranged from 78.5% to 86.9% among three imaging modalities. All modalities yielded
24 a PPV lower than 77.8% and a NPV higher than 90.0% in identifying the presence of malignant tumors. MRI presented a
25 diagnostic accuracy of 86.9%, as well as a sensitivity of 95.5% and an area under curve (AUC) of 0.948, which are higher
26 than mammography and ultrasonography.
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27 CONCLUSION: By using a diverse dataset and comparing the diagnostic accuracy of three imaging modalities commonly
28 used in breast cancer detection and diagnosis, this study also demonstrated that mammography, ultrasonography and MRI
29 had different diagnostic performance in breast tumor identification. Among them, MRI yielded the highest performance even
30 though the unexpected specificity may lead to over-diagnosis, and ultrosonography is slightly better than mammography.
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31 Keywords: Mammography, ultrasonography, breast magnetic resonance imaging (MRI), breast cancer diagnosis, diagnostic
32 performance assessment


Corresponding authors: Hong Li, Sino-Dutch Biomedical and Information Engineering School, Northeastern University,
195 Chuangxin Road, Shenyang, Liaoning, 110169, China. Tel.: +86 13889202825; E-mail: lihong@126.com.

0895-3996/18/$35.00 © 2018 – IOS Press and the authors. All rights reserved
2 H. Sun et al. / Performance evaluation of breast cancer diagnosis

32 1. Introduction

33 The incidence of breast cancer has increased globally in women over the last several decades. Despite
34 progress in identifying risk factors and genetic markers for breast cancer, most cases occur without
35 known major predictors [1, 2]. Tumour stage at detection is the key factor for survival. Breast imaging
36 has been recommended as a method of early diagnosis and confer benefits of reducing breast cancer
37 mortality in the population [3, 4]. Mammography, ultrasonography and MRI have been widely utilized
as noninvasive diagnostic imaging in clinical practice for evaluation of breast lesions.

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Accurate classification using medical images not only helps the physicians make the appropriate

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40 clinical decision on further examination and treatment, but also can reduce the economic burden of
41 patients. Performance evaluation of the three modalities can provide references for radiologists in
42 clinical diagnosis [5, 6]. Hongda Shao et al. evaluated the three modalities performance and MRI was
43 best with a sensitivity of 90.9%, a specificity of 82.7%, a PPV of 89.3%, a NPV of 85.3 and AUC of 0.88

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44 [6]. Juan Wang et al. proved MRI sensitivity (87.2%) were significantly higher than mammography
45 (76.9%) or ultrasonography (82.1) and MRI can detect most of small breast tumor (< = 2 cm) [7]. Berg
46 WA, et al. compared the advantages and disadvantages of three modalities in diagnosing different
47 types of breast diseases [8]. Strobel K, et al. calculated parameters to evaluated the three modalities

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48 performance as BI-RADS category 4 and gave the results that MRI was useful for the noninvasive
49 work-up of lesions classified at mammography or ultrasonography [9, 10].
50 In this article, we conducted a systematic comparative cohort study, investigating the diagnostic
51 accuracy, PPV, NPV, sensitivity, specificity, AUC and ROC space of mammography, ultrasonography
and MRI in the diagnosis of breast lesions. Through our study, the diagnosis performance of clinical
52
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53 suspected breast tumor by using these three modalities will be quantitatively evaluated. Moreover, our
54 dataset has the following characteristics comparing to the previous works. Firstly, the age range of
55 patients in our study is wide, from 19 to 62. Secondly, the dataset includes as many as 15 types of
56 breast diseases, i.e., breast adenosis, mastitis, abscess, granulomatous lobular mastitis(GLM), plasma
cell mastitis, fibroadenoma, phyllodes tumors, hyperplasia, intraductal papilloma, epidermal cysts,
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58 invasive ductal carcinoma (IDC), ductal carcinoma in situ (DCIS), invasive lobular adenocarcinoma,
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59 tubular carcinoma, and mucinous adenocarcinoma.

60 2. Materials and methods


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61 2.1. Participants

62 The retrospective study was conducted on 107 patients with suspected breast cancer (based on
63 findings such as pain, breast nipple discharge, palpable breast lumps and so on) between September
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64 2010 and July 2017. These data were obtained from cooperative hospital. The patients who had
65 completed the examinations of all three imaging modalities during the period were collected. Statistics
66 show that 90 patients finished the three inspections in a randomized order within one month, and
17 patients finished more than one month. The age of the participants ranged from 19 to 62 (mean
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68 37.3 ± 9.3 years old).

69 2.2. Imaging methods

70 Full-field digital mammography including two standard views, mediolateral oblique and craniocau-
71 dal had been performed by FDR-3000AWS of FUJIFILM. All images were acquired for each breast
72 through fully automated exposure control. Breast ultrasonography had been performed by voluson e8
73 of GE. All of the cases had undergone the breast MRI in the device Signa HDxt, GE. A conventional
H. Sun et al. / Performance evaluation of breast cancer diagnosis 3

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Fig. 1. Histogram of participants ages statistics.

Table 1
Image acquisition parameters of mammography, ultrasonography and MRI
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Modality Device Major parameters
mammography FUJIFILM KVP 31
FDR-3000AWS Field of View Dimension(s) 296/236
Exposure Time 810
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Tube Current 103


Image Pixel Spacing 0.05/0.05
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ultrasonography GE probe: LA523


voluson e8 frequency: 5–10 MHz
MRI GE, T1: TR 360 ms, TE 7.43 ms, section thickness 4.5 mm, FOV
340 mm, matrix 512 × 512, NEX 0.5
Signa HDxt T2: TR 5080 ms, TE 100.8 ms, section thickness 4.5 mm,
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FOV 340 mm, matrix 512 × 512, NEX 3


DWI: TR 4000 ms, TE 82.1 ms, section thickness 4.5 mm,
FOV 340 mm, matrix 256 × 256, NEX 4, b values
800 s/mm2
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MASK
DCE-MRI (eight sequences,)
DCE-subtracted images: DCE-MRI subtracting MASK
SCREENSAVE: increasing, plateau, washout
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74 breast MRI protocol was utilized using a standard breast coil in the prone position. Major parameters
75 of the different imaging modalities are shown in Table 1.
76 Imaging assessment score had been given based on BI-RADS criterion. Diagnosis were divided into
77 five categories: 1 (negative), 2 (benign finding), 3 (probably benign finding, short–term sustained moni-
78 tor), 4A (2–10% malignancy, biopsy recommended), 4B (10–50% malignancy, biopsy recommended),
79 4C (50–95% malignancy, biopsy recommended) and 5 (highly suggestive of malignancy) [11, 12].
4 H. Sun et al. / Performance evaluation of breast cancer diagnosis

Table 2
Probability range for the different imaging modalities in the entire cohort

BI-RADS Benign Probability (%) Malignant Probability (%)


category 1–2 100 0
category 3 99 (98–100) 1 (0–2)
category 4A 94 (90–98) 6 (2–10)
category 4B 70 (50–90) 30 (10–50)

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category 4C 27.5 (5–50) 72.5 (50–95)

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category 5 2.5 (0–5) 97.5 (95–100)

Note: B denotes benign breast lesion, M denotes malignant breast lesion.

80 2.3. Data analysis

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81 Common diagnostic parameters such as sensitivity, specificity, accuracy, PPV, NPV, AUC and ROC
82 space values were calculated by using 2 × 2 contingency tables, which were constructed by comparing
83 diagnostic outcome from three modalities with biopsy result which can be regarded as the golden
standard. ROC curve illustrates the performance of a binary classifier model as its discrimination

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85 threshold is varied [13]. When describing the ROC curve, we mapped the BI-RADS category into an
86 exact prediction either as positive or negative based on a certain threshold.
87 Based on BI-RADS criterion, each category corresponds to probability range of benign and malignant
88 (Table 2). According to TP, FP, TN and FN calculation methods, the median of the probability range is
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89 multiplied by the number of cases on a certain category, then the calculated values of all categories are
90 added, and we can get the sensitivity and specificity values for different imaging modalities to draw
91 the ROC space.
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92 3. Results
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93 According to the pathological reports, among 107 cases detected with the suspected breast cancer,
94 63 cases were categorized as benign lesions, including hyperplasia (22), breast adenosis (21), mastitis
95 (6), fibroadenoma (5), GLM (3), phyllodes tumors (2), abscess (1), plasma cell mastitis (1), intraductal
96 papilloma (1), epidermal cysts (1); while 44 cases were categorized as malignant lesions, including IDC
(36), DCIS (4), invasive lobular adenocarcinoma (2), tubular carcinoma (1), mucinous adenocarcinoma
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98 (1). Diagnosis results of BI-RADS category with mammography, ultrasonography and MRI modalities
99 compared to the pathological diagnosis are shown in Fig. 2.
100 Data analysis of case diagnosis results shows that each modality has its strengths and weaknesses. Fig-
ure 3 shows some examples. Mammography occurred misdiagnosis and overdiagnosis on the lesions
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102 with extremely dense or heterogeneously dense breasts, which were correctly diagnosed by ultra-
103 sonography and MRI. For a 45-year-old woman with adenosis in left breast (Fig. 3(a)), mammography
104 misdiagnosed as BI-RADS category 4B, but ultrasonography and MRI diagnosed as BI-RADS cate-
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105 gory 2 correctly. Relatively, the second example is a rare case. For a 27-year-old woman with breast
106 adenosis in left breast (Fig. 3(b)), the ultrasonography misdiagnosed as BI-RADS category 4B and 4A,
107 but mammography correctly diagnosed as BI-RADS category 1 because of extremely dense. Study
108 showed that ultrasonography diagnosis of fibroadenoma is better than mammography and MRI. How-
109 ever, ultrasonography may misdiagnose when lesions emerged glandular structural disorder. In the last
110 example (Fig. 3(c)), pathological diagnosis was IDC, ultrasonography deemed the lesion as BI-RADS
111 category 2 because this case was glandular structural disorder, however, MRI diagnosed as BI-RADS
112 category 4A and mammography diagnosed as BI-RADS category 4B.
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Fig. 2. Comparison between three imaging modalities and pathological diagnosis in 107 cases.

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Table 3
Correctly diagnosed, misdiagnosis and over-diagnosis numbers by three imaging modalities

Correctly diagnosed Misdiagnosis Overdiagnosis


mammography 84 3 20
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ultrasonography 90 4 13
MRI 96 0 11
mammography & ultrasonography 72 1 2
mammography & MRI 78 0 4
ultrasonography & MRI 81 0 1
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mammography & ultrasonography & MRI 69 0 2


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113 To illustrate the diagnosis performance of three modalities more clearly, the number of cases which
114 were diagnosed correctly, misdiagnosis and overdiagnosis by all three modalities, two modalities and
only one modality were systematically analyzed (Table 3).
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115

116 The ROC curve and the ROC space of three modalities was shown respectively in Fig. 4. The
117 diagnostic accuracy, PPV, NPV, sensitivity, specificity and AUC values of different imaging methods
118 in breast cancer diagnosis were shown in Table 4. It can be seen that the sensitivity of MRI was
significantly higher than mammography and ultrasonography. The AUC value of MRI can reach 0.948,
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120 which was higher than that of mammography and ultrasonography. However, the NPV value of MRI
121 was higher than that of mammography and ultrasonography, because the overdiagnosis rate of MRI
122 was the highest.
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123 Figure 4 shows and compares three unsmoothed ROC curves generated using three imaging modali-
124 ties in classifying between malignant and benign breast tumors. It shows that using MRI yielded highest
125 AUC value, while using mammography generated smallest AUC value. In addition, by applying an
126 operating threshold to three imaging modalities, three performance markers are also plotted in Fig. 4,
127 which show that MRI yields the significantly higher TPR (68.1%) than mammography (53.8%) and
128 ultrasonography (59.7%) in the diagnosis of breast cancer, but the FPR value of MRI (10.0%) is the
129 middle of the three modalities namely, the FPR values are 10.7% and 9.4% for mammography and
130 ultrasonography, respectively.
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Fig. 3. Row from left to right: medial lateral oblique mammography, craniocaudal mammography, DCE-MRI, ultrasonog-
raphy. Three cases of each column from top to bottom: (a) the 45-year-old woman with adenosis in left breast; (b) the
27-year-old woman with adenosis in left breast; (c) the 60-year-old woman with IDC in left breast.
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Table 4
Diagnostic value of different imaging modalities in the entire cohort

Imaging methods Sensitivity (%) Specificity (%) PPV (%) NPV (%) Accuracy (%) AUC
mammography 88.6 71.4 68.4 90.0 78.5 0.877
ultrasonography 90.9 79.4 75.5 92.6 84.1 0.919
MRI 95.5 81.0 77.8 96.2 86.9 0.948

Note: p < 0.0001 is accepted as statistically significant. All results based on 95% CI.
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Fig. 4. ROC curve and ROC space of mammography, ultrasound and MRI.

131 4. Discussion
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132 Although many new investigative imaging modalities have been developed and tested in breast cancer
133 detection and diagnosis (i.e., different types of CT-guided imaging modalities [14, 15]), mammography
134 remains the standard examination imaging modality used in breast cancer screening of the general
135 population in current clinical practice [16]. However, our study shows that using mammography cannot
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136 easily detect non-calcified lesions especially when the lesions are located within extremely dense
137 or heterogeneously dense breast tissue, so misdiagnosis can happen. Relatively, mammography can
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138 accurately diagnose when breast tissue belongs to entirely fatty and scattered areas of fibroglandular
139 density.
140 Ultrasonography has been commonly used as an imaging procedure where mammography and MRI
141 are not available in some clinics. It can identify small nonpalpable masses in dense breast tissue whereas
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142 mammography cannot detect it well. Among all of the lesions in our dataset, two cases of benign lesions
143 in dense breasts were misdiagnosed by mammography but correctly diagnosed by ultrasonography.
144 Meanwhile, one case of malignant lesions in dense breasts were misdiagnosed by mammography but
145 correctly diagnosed by ultrasonography. However, the sonogrsphic features of benign and malignant
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146 breast lesions have some overlaps, so ultrasonography diagnostic specificity is low [17, 18]. In our
147 dataset, ultrasonography misdiagnosed two cases as malignant which pathological results were benign.
148 In addition, ultrasonography is an operator-dependent technique, so it has never been used as the only
modality for breast cancer screening [19–21].
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150 MRI includes many scan protocols so that it can yield significant improvement in cancer diagno-
151 sis. Our results indicated that both the sensitivity and the AUC of MRI were higher than those of
152 mammography and ultrasonography, which is consistent with most previous reported work [22–24].
153 MRI has a higher accuracy than mammography and ultrasonography in detecting malignant tumor,
154 but it misdiagnosed as BI-RADS category 4 easily on some benign lesions, such as breast adenosis,
155 phyllodes tumors, hyperplasia and lobular inflammation. In our dataset, twelve cases were overdiag-
156 nosed malignant by MRI, but their pathological results were benign. It indicated that MRI reduced the
157 specificity performance. Moreover, high examination cost may limit its use widely [6, 25, 26].
8 H. Sun et al. / Performance evaluation of breast cancer diagnosis

158 Comparing with previous work from Hongda Shao et al. [6], Juan Wang, et al. [7], Berg WA,
159 et al. [8] and Strobel K, et al. [9], our study presented more performance evaluation values. Firstly, the
160 patients in our study have a wide range of age, and there were 65 cases under 35 years old. Secondly,
161 our study involved more types of diseases (10 types of benign lesions and 5 types of malignant tumor),
162 which makes the results more representative. Thirdly, our evaluation method was comprehensive, and
163 seven measures were employed. The ROC curve could present the results intuitively and the ROC
164 space was proposed.

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165 From our study, both mammography and MRI have high clinical value in diagnosis of breast tumor.

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166 Furthermore, MRI can provide more information and its diagnosis sensitivity is higher than mammog-
167 raphy. So MRI, with a higher clinical value, is worth promoting. Ultrasonography plays important role
168 for the early diagnosis of dense breasts. In particular, ultrasonography check-up doesn’t involve radia-
169 tion. Besides images, radiologists may need additional information like age, family history, menopause
170 and so on to finish their diagnosis. For high-risk populations including the subjects with the family

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171 history of breast cancer or suffered from cervical cancer, it suggested that the combined MRI and mam-
172 mography can be the choice for early detection of breast cancer. Even so, none of ultrasonography,
173 mammography and MRI can replace pathological surgery in the detection of breast carcinoma now,
174 because none of those three modalities reaches the criterion of 100% sensitivity and 100% specificity.

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175 That means although measures can be taken to improve the accuracy, the gap between medical imaging
176 methods and pathological golden standard will still exist for some time.

ACKNOWLEDGMENTS
177
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178 The scientific guarantor of this publication is Prof. Wei Qian. The authors of this manuscript declare
179 no relationships with any companies whose products or services may be related to the subject matter
180 of the article. This study was funded by the National Key Research and Development Program Sub
– topics under Grant (No. 2016YFC1303005), the Natural Science Foundation of Liaoning Province
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182 of China under Grant (No. 201404186), the Fundamental Research Funds for the Central Universi-
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183 ties under Grant (No. N150408001), the National Natural Science Foundation of China under Grant
184 (No.81671773, 61672146). The ethics committee of Shengjing Hospital of China Medical University
185 (Number: 2014PS67K). Methodology: retrospective, diagnostic or prognostic study, performed at one
186 institution.
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