Background The resection volume in relation to the breast volume is known to inﬂuence cosmetic outcome fol- lowing breast-conserving therapy. It was hypothesised that three-dimensional ultrasonography (3-D US) could be used to preoperatively assess breast and tumour volume and show high association with histopathological measurements. Methods Breast volume by the 3D-US was compared to the water displacement method (WDM), mastectomy specimen weight, 3-D MRI and three different calculations for breast volume on mammography. Tumour volume by the 3-D US was compared to the histopathological tumour volume and 3-D MRI. Relatedness was based on the intraclass correlation coefﬁcient (ICC) with corresponding 95% conﬁdence interval (95% CI). Bland–Altman plots were used to graphically display the agreement for the different assessment techniques. All measurements were performed by one observer. Results A total of 36 patients were included, 20 and 23 for the evaluation of breast and tumour volume (ductal invasive carcinomas), respectively. 3-D US breast volume showed ‘excellent’ association with WDM, ICC 0.92 [95% CI (0.80–0.97)]. 3-D US tumour volume showed a ‘excellent’ association with histopathological tumour volume, ICC 0.78 [95% CI (0.55–0.91)]. Bland–Altman plots showed an increased overestimation in lager tumour volumes measured by 3-D MRI compared to histopathological volume. Conclusions 3-D US showed a high association with gold standard WDM for the preoperative assessment of breast volume and the histopathological measurement of tumour volume. 3-D US is an patient-friendly preoperative available technique to calculate both breast volume and tumour volume. Volume measurements are promising in outcome prediction of intended breast-conserving treatment. Introduction & M. Lagendijk firstname.lastname@example.org For early stage breast cancer, similar survival rates are Department of Surgical Oncology, Erasmus MC Cancer obtained when performing a mastectomy or breast-con- Institute, Groene Hilledijk 301, 3075 EA Rotterdam, serving therapy (i.e. partial removal of the breast followed The Netherlands by whole breast irradiation; BCT) . Considering the high Department of Bio-informatics, Erasmus MC, survival rates , (surgical) treatment decisions should ‘s-Gravendijkwal 230, 3015 CE Rotterdam, The Netherlands focus on health-related quality of life in addition to the Department of Radiology, Erasmus MC, ‘s-Gravendijkwal oncological outcomes. The type of surgery performed 230, 3015 CE Rotterdam, The Netherlands inﬂuences health-related quality of life . In order to Department of Surgical Oncology, Erasmus MC Cancer improve cosmetic outcome following BCT, multiple Institute, PO Box 5201, 3008 AE Rotterdam, The Netherlands 123 2088 World J Surg (2018) 42:2087–2093 studies have focused on (preoperative) radiological imag- measurement where those scheduled for BCT were eligible ing to predict or improve the cosmetic outcome [4, 5]. for tumour volume measurement. All measurements were One of these preoperative parameters is breast volume, performed by one observer. commonly assessed in the area of breast reconstructive surgery . Preoperative breast volume measurements Histopathological evaluation have been described using various three-dimensional (3-D) techniques [6–10]. These techniques showed high concor- Breast volume (N = 20) was measured on freshly excised dance for the preoperatively accessed breast volume in breast specimen using two techniques. Primarily, the water comparison to the water displacement method (WDM or displacement method (WDM) was used intraoperatively. Archimedes’ method). The WDM is considered the gold WDM is based on Archimedes’ theory and considered gold standard for breast volume measurement, but is only standard [9, 11]. The mastectomy specimen was submerged available following resection [9, 11]. into a graduated cup partly ﬁlled with water. The displaced Tumour volume studied as preoperative parameter has water is than equal to the volume of the specimen. Second been described to predict the expected resection volume the breast volume was calculated by multiplying the [11–13]. The resection volume in BCT is known to inﬂu- specimen weight (gram) by the molecular weight, esti- ence cosmetic outcome [13–16]. Tumour volume mea- mated to be 0.958 g/cm . This molecular weight surement can be performed on both mammography and resembles the situation where the breast consists of 50% breast ultrasonography [11–13]. No gold standard is fatty tissue and 50% ﬁbro-glandular tissue. available for the preoperative assessment of tumour vol- Tumour volume (N = 23) was calculated assuming the ume. In the postoperative setting the gold standard for tumour to resemble an obloid spheroid (Fig. 1). Three tumor volume is the volume as based on the freshly excised diameters of the carcinoma were obtained on the fresh tissue. tissue specimen. If ductal carcinoma in situ (DCIS) was The tumour volume-to-breast volume ratio in combina- present in the direct surrounding of the invasive compo- tion with the quadrant of the breast where the tumour is nent, the longest diameter of this area was additionally located is expected to be predictive for the cosmetic outcome obtained. If a DCIS component was larger than 1.5 cm, following BCT . A precise measurement of both tumour patients were categorised as ‘DCIS [ 1.5’. If a DCIS and breast volume is needed to enable this preoperative component was smaller than 1.5 cm, patients were cate- prediction of the expected cosmetic outcome following gorised as ‘DCIS \ 1.5’. BCT. To access these volumes, a ultrasonography was chosen since it has several advantages over the use of other Preoperative imaging radiological modalities: it is widely available, affordable, non-invasive and does not depend on ionising radiation as Automated breast volume scanner (ABVS) (3-D US) compared to a mammography. It was hypothesised that 3-D US could be used to measure breast and tumour volume and 3-D US was performed using the Siemens Automated TM furthermore shows a good association with histopathological Breast Volume Scanner (ABVS—ACUSON S2000 volumes. For this the ultrasound volume was compared to the ABVS, Siemens Medical Solutions, Inc, Mountain View, WDM, histopathological mastectomy specimen weight, 3-D CA) . The ABVS uses a linear transducer (17 cm) that MRI and mammography for breast volume and the automatically scans the breast in 60 s. Total breast volume histopathological tumour volume, 3-D MRI and mammog- was captured conducting three or ﬁve scans per breast raphy for tumour volume. based on size of the breast (i.e. anterior–posterior, lateral Materials and methods This prospective study was approved by the Ethics Com- mittee of the Erasmus MC. Patients operated between March 2015 and December 2015 with a preoperative breast MRI were included prior to surgery after written informed consent was obtained. Since the study is considered an feasibility study, no power analysis was performed. Patients undergoing a mastectomy were eligible for breast and tumour volume measurement. Patients undergoing a Fig. 1 Mammographic determination of tumour volume  prophylactic mastectomy were eligible for breast volume 123 World J Surg (2018) 42:2087–2093 2089 and medial or anterior–posterior, upper-lateral, lower-lat- medio-lateral-oblique  or a combination of the two eral, upper-medial and lower-medial). Ultrasonography ) are used for this second formula. data were analysed using a virtual reality desktop system Breast volume half - elliptic shape ¼ðÞ p=4 hwc ð1Þ developed by the department of Bioinformatics, Erasmus Breast volume circular cone ¼ 1=3 pr h ð2Þ MC, running the V-Scope software . This software enables volume measurements in a 3-D-plane by display- Tumour volume was measured considering the tumour ing the ABVS data on a virtual reality desktop system. as an obloid spheroid equal to the tumour volume measured Data can then be manipulated with a 3-D-mouse and during histopathological evaluation (Fig. 1). wireless pointer. Calculations were based on differences found in grey levels (echogenicity). Data analysis 3-D breast MRI Data were analysed using IBM SPSS Statistics (126.96.36.199). 3 3 The median breast volume (cm ) and tumour volume (cm ) Contrast enhanced-MRI data were analysed using the with corresponding interquartile ranges were obtained per V-Scope software in a four-walled CAVE Automatic Vir- modality. The single measure intraclass correlation coef- tual Environment I-Space system (Barco NV, Kortrijk, ﬁcient (ICC) with 95% conﬁdence interval was used to Belgium). Here eight projectors create an interactive calculate the measure of reliability between the different hologram enabling manipulations with a wireless joystick. measurement techniques. For the interpretation of the Volumes were calculated based on differences in grey reliability, an ICC of\0.40 ‘Poor’, an ICC of 0.40–0.59 as levels representing different anatomical structures . ‘Fair’, an ICC of 0.60–0.74 as ‘Good’, an ICC of 0.74–1.00 as ‘Excellent’ . All breast volume measurement was Mammography compared to the WDM (gold standard). For tumour vol- ume, a comparison was made to the volume measured on Breast volume by mammography was measured based on freshly excised specimens. Bland–Altman plots were used two formulas (see below). The ﬁrst equation considers the to visualise the accuracy for the preoperative breast volume breast as a half-elliptic shape and accounts for the com- and tumour volume techniques compared to histopatho- pression force of the breast (Fig. 2a) . The height (h) logical volume. The y-axis displays the absolute difference and width (w) of the base of the breast were measured in a between the two techniques (technique A – B), and the x- medio-lateral-oblique view of the mammography. The axis displays the averaged volume of the two techniques compression during the mammography was encountered in (technique (A ? B)/2). The corresponding limits of the formula as ‘c’, which is expressed as the compression agreement are graphically displayed to evaluate the dif- in millimetres. The second measurement considers the ference in relation to the breast or tumour volume (i.e. the breast to best resemble a circular cone (Fig. 2b). The height upper and lower limit representing the boundaries of the of the breast was expressed as ‘h’, and the width of the base 95% conﬁdence interval). of the breast was expressed as ‘r’. In literature, available different mammography views (i.e. cranio-caudal , Fig. 2 Mammographic determination of breast volume. a Breast volume as a elliptic shape . b Breast volume as a circular cone [15, 17, 23] 123 2090 World J Surg (2018) 42:2087–2093 Results A total of 20 and 23 specimens were used for the evalua- tion of breast and tumour volume, respectively. Median breast volume measured by WDM (gold standard) was 462 cm [interquartile range, IQR (300–850)] (Table 1). All carcinomas available in the study were ductal carci- nomas. Median tumour volume measured by histopatho- logical evaluation was 1.33 cm [IQR (0.42–3.28)] (Table 1). Breast volume 3-D US showed an ‘excellent’ association with the WDM, intraclass correlation coefﬁcient (ICC) 0.92 [95% CI (0.80–0.97)] (Table 2). 3-D MRI, mammographic breast volume by Kalbhen, Katariya, Fung and Cochrane addi- tionally showed an ‘excellent’ association with the WDM, ICC 0.95 [95% CI (0.87–0.98)], 0.91 [95% CI (0.77–0.97)], 0.90 [95% CI (0.75–0.96)] and 0.81 [95% CI (0.55–0.93)], respectively (Table 2). Agreements for WDM with 3-D US, 3-D MRI and mammographic breast volume by Kalbhen (MxKalbhen) are graphically displayed by Bland–Altman plots (Fig. 3). It is shown that the dif- ferences for the two techniques fall mainly between the limits of agreement. For the 3-D MRI, a substantial increase in the overestimation is seen with an increasing breast volume (Fig. 3b). Tumour volume 3-D US showed ‘excellent’ association with histopatho- logical tumour volume, ICC 0.78 [95% CI (0.55–0.91)] (Table 3). 3-D MRI showed a ‘good’ association with histopathological tumour volume, ICC of 0.73 [95% CI Table 1 Median volume (cm ) (interquartile range) Breast volume (n = 20) (cm ) Water displacement method (WDM) 462 (300–850) Breast volume by molecular weight 432 (350–676) 3-D US 427 (315–779) 3-D MRI 550 (436–1175) MxKalbhen 575 (438–681) MxCochrane 809 (706–1019) MxFung 766 (614–1000) MxKatariya 742 (559–1000) Tumour volume (n = 23) (cm ) Histopathological tumour volume 1.33 (0.42–3.28) 3-D US 1.15 (0.43–1.79) 3-D MRI 2.24 (0.97–3.97) US ultrasound, Mx mammography Table 2 Intraclass correlation coefﬁcient (95% conﬁdence interval) for breast volume measurements WDM Molecular weight 3-D US 3-D MRI MxKalbhen MxKatariya MxFung Molecular weight 0.95 (0.87–0.98) 3-D US 0.92 (0.80–0.97) 0.96 (0.91–0.99) 3-D MRI 0.91 (0.78–0.96) 0.90 (0.76–0.96) 0.92 (0.81–0.97) MxKalbhen 0.92 (0.79–0.97) 0.94 (0.83–0.98) 0.90 (0.73–0.96) 0.86 (0.64–0.95) MxKatariya 0.91 (0.77–0.97) 0.94 (0.83–0.98) 0.92 (0.80–0.97) 0.94 (0.84–0.98) 0.88 (0.71–0.96) MxFung 0.90 (0.75–0.96) 0.96 (0.89–0.99) 0.93 (0.81–0.97) 0.94 (0.83–0.98) 0.94 (0.84–0.98) 0.95 (0.87–0.98) MxCochrane 0.81 (0.55–0.93) 0.88 (0.71–0.96) 0.84 (0.61–0.94) 0.85 (0.64–0.94) 0.89 (0.72–0.96) 0.83 (0.59–0.93) 0.95 (0.87–0.98) WDM water displacement method, US ultrasound, Mx mammography, Mx Kalbhen mammographic breast volume calculated based on Kalbhen’s technique, Mx Katariya mammographic breast volume calculated based on Katariya’s technique, MxFung mammographic breast volume calculated based on Fung’s technique ICC of \ 0.40 ‘Poor’, an ICC of 0.40–0.59 as ‘Fair’, an ICC of 0.60–0.74 as ‘Good’, an ICC of 0.74–1.00 as ‘Excellent’  World J Surg (2018) 42:2087–2093 2091 Fig. 3 Bland–Altman plots for breast volume with the mean (WDM - 3-D US) as a function of the volume ((WDM ? 3-D difference (solid line) and limits of agreement (dotted line). US)/2). b Mean difference (WDM - 3-D MRI) as a function of the BV = breast volume, WDM = water displacement method, volume (WDM ? 3-D MRI). c Mean difference (WDM - MxKalb- US = ultrasound, Mx = mammography. a Mean difference hen) as a function of the volume ((WDM ? MxKalbhen)/2) histopathological tumour volume and 3-D US and 3-D MRI Table 3 Intraclass correlation coefﬁcient (95% conﬁdence interval) are graphically displayed by Bland–Altman plots (Fig. 4). for tumour volume measurements Differences between the techniques fall within the limits of Histopathological tumour volume 3-D US agreement except for one measurement. Ten patients (43.5%) had more than 1.5 cm diameter of 3-D US 0.78 (0.55–0.91) ductal carcinoma in situ (DCIS) and were considered as 3-D MRI 0.73 (0.44–0.88) 0.94 (0.87–0.98) ‘DCIS [ 1.5’. For the ‘DCIS [ 1.5’ group ‘Poor’ relia- TV tumour volume, US ultrasound bility scores were found for both 3-D US and 3-D MRI ICC of \ 0.40 ‘Poor’, an ICC of 0.40–0.59 as ‘Fair’, an ICC of with histopathological tumour volume, ICC, respectively, 0.60–0.74 as ‘Good’, an ICC of 0.74–1.00 as ‘Excellent’  0.01 [95% CI (-0.64 to 0.63)] and 0.04 [95% CI (-0.61 to 0.66)]. For the ‘DCIS \ 1.5’ group the association for 3-D US and 3-D MRI with histopathological tumour volume (0.44–0.88)] (Table 3). Mammographic assessment of was ‘Excellent, ICC 0.86 [95% CI (0.57–0.96)] and ICC tumour volume was discarded since only in 14/23 (60.8%) 0.88 [95% CI (0.63–0.96)], respectively. tumour volume could be assessed. Agreements for Fig. 4 Bland–Altman plots tumour volume with the mean difference function of the volume ((PA ? 3-D US)/2). b Mean difference (solid line) and limits of agreement (dotted line). TV = tumour (PA - 3-D MRI) as a function of the volume ((PA ? 3-D MRI)/2) volume, US = ultrasound. a Mean difference (PA - 3-D US) as a 123 2092 World J Surg (2018) 42:2087–2093 is often not visible on ultrasonography as compared to the Discussion contrast enhanced 3-D MRI images [26, 27]. To evaluate Breast volume measurement by 3-D US as well as by the accuracy for both 3-D US and 3-D MRI, a differenti- ation was made in the histopathological evaluation for the Kalbhen mammography shows an ‘excellent’ association with gold standard water displacement method (WDM) invasive component (visible on ultrasonography) and for the amount of DCIS. A subgroup analysis, evaluating only with ICC of 0.92 and 0.95, respectively. Tumour volume measurement by 3-D US shows ‘excellent’ association with patients without DCIS, was not performed due to a limited patient number (n = 7). It is however expected to show an histopathological tumour volume (ICC 0.78). The impor- tance of breast volume and tumour volume measurements ‘excellent’ association with tumor volume as seen in patients \1.5 cm DCIS. It is uncertain if the chosen dif- preoperatively could be the cosmetic outcome prediction of ferentiation between\1.5 cm DCIS and[1.5 cm DCIS is breast-conserving treatment. In literature, volume mea- an accurate cut-off value which forms a limitation of the surements indeed enabled preoperative evaluation of the study. The preoperative calculation of the tumour volume expected resection volume in ratio with the breast volume and thus a possible prediction of the expected cosmetic in the presence of a known or expected large diameter of DCIS should be performed with caution. outcome [5, 13, 14]. Currently 3-D US is being used in a randomised controlled trial with the aim to preoperatively Overall 3-D US enables an accurate preoperative, patient-friendly breast volume assessment without the use predict whether BCT will generate a good cosmetic result based on the tumour volume-to-breast volume ratio (NTR of ionising radiation as in mammography. As conﬁrmed in our cohort, mammographic breast volume shows high 4997). relatedness with both the WDM  and breast volume by A strength of the current study is that volumes were mastectomy specimen weight technique [17, 22]. As a evaluated by all mentioned measurement techniques per preoperative technique, 3D-US is expected to be a suit- patient: WDM and histopathological tumour volume if able and patient-friendly alternative with equal high cor- applicable, 3-D US, 3-D MRI, and tumour volume by relation to the WDM technique as obtained by mammographic formulas. To our knowledge, this is the ﬁrst study to report on breast volume assessment using 3-D mammography. Tumour volume measured by ultrasound has been ABVS images. The availability of both breast volume and tumour volume measured on freshly excised specimens studied to preoperatively estimate the expected resection volume with high concordance to the histopathological enabled an accurate comparison. A limitation of the current study is that only ductal volume [12, 13]. Clauser et al.  showed high concor- dance comparing tumour volume by MRI with tumour carcinomas of the breast were available within the cohort. It is therefore uncertain if results for tumour volume are volume by hand-held ultrasonography and histopathologi- cal tumour volume. Various studies, however, showed an generalisable for other histological subtypes. Mammogra- overestimation of the tumour volume by MRI [28–30]. phy was considered unsuitable as a preoperative technique to access tumour volume at the time of evaluation; no This overestimation was conﬁrmed within our cohort as presented by the Bland–Altman plot (Fig. 4) and can pos- tomography was available that could have possibly increased tumour visibility in dense breast tissue. The sibly be explained by the contrast enhancement images which colour the surrounding of the tumour or the presence interpretation of the intraclass correlation coefﬁcient (ICC) to rate the level of reliability varies in literature of DCIS (as shown by the overall larger tumour volumes measured by MRI). As shown in the Bland–Altman anal- [11, 24, 25], making an unambiguous interpretation more difﬁcult. Martins  suggested much higher cut-off val- ysis, 3-D US is more accurate in predicting histopatho- logical tumour volume than 3-D MRI when smaller lesions ues when interpreting the reliability of ultrasound in foetal are evaluated. As expected, 3-D MRI showed better relat- measurements. Clauser et al. , however, used compa- edness to histopathological tumour volume in the presence rable cut-off values for their interpretation of the reliability of DCIS if\1.5 cm in the direct surrounding of the tumour of a 3-D US in breast cancer patients without referring to their guide for interpretation. Although different cut-off (ICC 3-D MRI 0.88 compared to ICC 3-D US 0.86 both in relation to histopathological volume). values are used, it should be taken into account that the ICC is dependent on the total variance found in the samples In conclusion, breast volume can accurately be assessed by mammography based on Kalbhen’s technique or by 3D- and should therefore be interpreted in the clinical setting used. US which forms a more patient-friendly alternative. Tumour volume (with limited DCIS) measurement by 3D- The precise differentiation between the invasive com- ponent and DCIS on histopathology enabled judgment on US and 3D-MRI was comparably adequate with ‘excellent’ to ‘good’ relatedness for histopathology. Future research the performance of both 3-D US and 3-D MRI since DCIS should further evaluate the use of preoperative volume 123 World J Surg (2018) 42:2087–2093 2093 12. 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World Journal of Surgery – Springer Journals
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