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Background: Neoadjunvant chemotherapy has become a challenging connotation for both surgeons and radiolo- gists due to the high clinical response up to dramatic pathological complete response (pCR) that may hinder proper localization of any residual tumoral tissue. So the radiopaque markers implantation at the tumor bed became a reli- able and recommended method for tumor localization before surgical intervention or NAC. Many types of commer- cial clips and markers are available; however they are relatively of high cost and represent a considerable burden on the governments and the heath institute that made the researchers study cheaper alternatives as standard titanium based cholecystectomy surgical clips for tumor localization. Results: The study was conducted on 45 patients where 57 clips were inserted corresponding to number of lesions found in the total number of the patients. The response to Neoadjunvant chemotherapy was recorded and showed that 6 patients (about 13.3%) had complete radiological response after NAC, while 27 patients (60%) had regressive course after the treatment. The low cost surgical clips were evaluated by using sono-mammography and magnetic resonance imaging, and complications that occurred were recorded. Our study showed that in only 2 patients (3.5%) there was difficulty in clip visualization by Ultrasound during post-treatment follow up. In 45 patients, all the inserted clips (100%) were well visualized as small signal void on MRI at both T1WIs and T2WIs sequences, and the primary malignancy was easily visualized on both MRI and sono-mammography not interfering with the image interpreta- tion and judgment. As regards the reported complications, our results revealed that in only 2 patients (3.5%) there was evidence of positive clip migration, while only 2 patients (3.5%) developed hematoma during the procedure as shown by ultrasound, Also 4 patients (7%) complained of pain only shortly after clip insertion. No other significant complications like infection or heat sensation developed either during the procedure or during MRI. The total price of the surgical clips was calculated with average cost of the needle about 10 US$ equivalent to 170 LE Egyptian pounds and the clip about 1.3 US$ or 20 Egyptian pounds, which is considered of lower cost when compared to the commer- cial breast markers of different companies with an estimated price range for clip = 75–200 US$ (average 90 US$). So insertion of surgical clips saved about 1135 Egyptian pounds equivalent to 73–75 US$ per clip placement. Conclusion: We concluded from our study that the use of breast markers are mandatory before NAC where Surgical clips can safely substitute the commercial tissue markers as tumor localizers as they are effective, safe, well tolerated, *Correspondence: norhanmedecine@gmail.com Radio-Diagnosis Department, Faculty of Medicine, Ain Shams University, Cairo, Egypt © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Abdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 2 of 16 easily visualized on imaging and do not interfere with assessment of the treatment response, with no evidence of complications and are of low cost compared with the commercial breast clips. Keywords: Breast cancer, Neoadjunvant chemotherapy, Surgical clips Background cancer before the start of NAC or before surgical resec- Breast malignancy is one of commonest tumor affect - tion (even reconstructive surgery) in patients who ing women, representing 31% of overall tumors affect - received NAC [2]. ing the female population. Also, 10% of the females Application of breast markers adds more progress in have the risk of developing breast cancer at some stage the field of interventional radiology in concerns with in their life [1], The rate of breast cancer in women is breast cancer as such clips are inserted using the ultra- increasing each year while the age at initial diagnosis sound-guided technique [5]. is shifting to a younger age and the increase in breast Although there are many types of commercial clips cancer incidence is accompanied by an increase in the and markers: however, they are relatively expensive and clinician and researchers concerns in the improvement represent quite a considerable economic burden that of diagnostic and therapeutic tools [2]. encourages the researchers to search for other lower cost The treatment options determining the therapeutic alternatives such as titanium cholecystectomy surgical choice in primary breast cancer patients are becoming clips [5]. Titanium-based metallic clip markers are used variable. And new therapies are now added to the usual in many parts of the world for tumor localization and chemotherapy regimens resulting in dramatic change in they are placed within the tumor under image guidance the treatment strategies of breast cancer over the past either mammography or sonography [2]. decade [3]. Neoadjuvant chemotherapy (NAC) is now consid- Aim of the study ered the standard of care for breast cancer patients Our study aimed to investigate the feasibility and cost with operable or inoperable tumors [1], the values of effectiveness of using sonographically-guided indigenous NAC appeared in decreasing the mortality incidence, low-cost surgical clips as tumor localization markers by changing the surgical approach as the use of breast sonomamography and Magnetic resonance imaging, this conservative surgery (BCS) and converting the inoper- including their complications and influence on the imag - able lesions into operable ones. It also assisted in early ing assessment after NAC. detection of tumor response to therapy and tumor biol- ogy of breast cancers [4]. Patients and methods Multiple studies demonstrated high clinical response A prospective study conducted on patients who were rate to the NAC with success rates reaching to about referred to the Radiology Department, with pathologi- 80–90%. The response of breast cancer to NAC cally proved malignant breast lesion/s for clip insertion. assessed using pathologic complete remission (pCR) Inclusion criteria: and in some patients complete clinical, radiological and pathological response can be attained following NAC • All adult Female patients with histopathologically [2], this dramatic pCR may hinder proper localization proven breast carcinoma (BIRADS VI) who were of any residual tissue by the radiologists or the surgeon scheduled to undergo NAC with early stage disease [1]. were included (up to stage II). If complete tumor response can be achieved, accurate and reliable detection of the tumor bed after NACT by Exclusion criteria: radiology and pathology is required. The use of radi - odense marker clips has been shown to be an effective • Patients with locally advanced breast cancer or stage and reliable method to identify the region of interest. IV disease will be excluded. The clip can be detected by either ultrasound or mam - • Patients with a high bleeding profile or patients with mography, and wire marking of the already inserted clip no available histopathological data for the breast can be performed to guide the surgeon to the tumor lesions will be excluded from the study (Fig. 1). bed [2]. • Patients with contraindications to intravenous MRI For this reason, the international breast cancer spe- contrast administration, e.g.: allergic to IV contrast, cialist panel in 2006 and 2010 announces the impor- high serum creatinine, low GFR or severe renal tance of radiopaque marker localization into the breast impairment. A bdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 3 of 16 array breast coil with IV gadolinium injection with a Histopathology dose of 0.1 mmol/kg (or 0.2 mL/kg) and a flow rate of 80.0% 1–2 mL/s flushed by 20 mL of physiological saline. Slice 68.9% 70.0% thickness was less than or equal to 3 mm with pixel size 60.0% less than 1 mm on each side. Acquisition time was less than 2 min as the mean enhancement time of a malig- 50.0% nant tumour is between 90 and 120 s. Morphological 40.0% sequences was taken as follows: T2W-TSE (AXIAL), 30.0% T1W-TSE (AXIAL), STIR sequences (AXIAL), Dynamic 20.0% 13.3% T1-weighted gradient echo after IV gadolinium injec- 8.9% 10.0% 4.4% 4.4% tion, T1W-TSE + C, SAG-LT + C SENCE, SAG-RT + C 0.0% SENCE, COR + C SENCE, Diffusion-weighted imaging IDC Grade IIDC grade II IDC grade IIILocally IDC grade II (DWI SSh) and ADC. advanced with IDC micropaillary Images acquired were evaluated for the following pattern parameters: lesion morphology and extension, the degree Fig. 1 Histopathology distribution of the breast lesions among study of artifact exerted by the clips and its effect on charac - group terization of the lesion and location of clip. The initial and follow up by sono-mammography after finishing the NAC was performed by Logic P9 ultrasound • Patients with contraindications to MRI as: claustro- machine (GE—General Electric Healthcare—USA) with phobic patients, high grades of obesity may not be fit a high frequency linear array transducer 8–15 MHz with certain MRI machines, pace makers or metallic and senographe pristina, GE healthcare mammography artifact. machine with the mean time interval between the inser- • Recurrent cases and pregnant females. tion of the clip to preoperative follow up sonomammog- raphy was about 24 weeks ± 2 weeks (about 6 months or Ultrasound guided clip insertion was done using dis- after about 8 sessions of NAC). The follow up sonomam - posable Guillotine biopsy needle 14 G × 20 cm GTA , mography was assessed for: location of the clips and with continuous real-time scanning during needle place- exclusion of any complications as clip migration by com- ment (Fig. 2). The needle stylet is removed and fit single paring the distance of the clip to the last sonomamog- GRENA surgical titanium ligation clip into the bore of raphy done before NAC on three coordinate points on the needle transducer. The coaxial needle was advanced mammography film (distance from the nipple, from the along the anesthetized track. Attempts should be made skin and from the muscle), displacement was recorded to identify the needle as soon as it enters the breast. It if there was > 1 cm difference in the clip position, and is imperative to know where the tip of the needle is at all finally the effect of the clip on the image interpretation times, thereby precluding the possibility of inadvertent and the assessment of response to treatment according puncture of an unintended structure (i.e., the chest wall). to RECIST criteria (Response evaluation criteria in solid If the transducer and the needle maintain the same lon- tumors) (Tables 1, 2). gitudinal axis, complete needle visualization is ensured. Patients with lesions no more palpable by the surgeons The stylet was used to deploy the 2–4 mm titanium clip after the treatment were referred back to the Interven- into the center of the lesion followed by removal of the tion radiology department for pre-operative wire locali- biopsy needle with the stylet. The clip is inserted in the zation over the already placed clips. center of the lesion and if there were the multiple or Cost-effectiveness was determined by calculating the large breast cancers, additional clips were placed for cost of the surgical clips and that of the commercial lesion extent bracketing as per the radiologist’s judg- metallic markers, while cost saving was calculated by ment. Then sono-mammography was done immediately comparing the two values. after clip insertion for confirmation of the site of the clips and exclusion of any immediate complications, and after that the patients started neoadjunvant chemotherapy Statistical analysis regimen. Recorded data were analyzed using the statistical pack- Breast magnetic resonance examinations was per- age for social sciences, version 20.0 (SPSS Inc., Chi- formed at the start of the Neoadjunvant chemotherapy, cago, Illinois, USA). Quantitative data were expressed as using a 1.5 T machine (Achieva and Ingenia, Philips mean ± standard deviation (SD). Qualitative data were medical system, Eindhoven, Netherlands) using phased expressed as frequency and percentage. Abdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 4 of 16 Fig. 2 Schematic diagram of the preoperative ultrasonography (US) guided surgical clip insertion. A The coaxial guiding needle with an inner stylet and surgical clips. B Under US-guidance (blue), the coaxial guiding needle (white) is inserted into the center of the breast cancer (pink), and one or two clips (black) are passed through. The inner stylet (light blue) is reinserted for pushing the clip (Quoted from Young et al. [1]) The following tests were done: Table 2 Ultrasound clip assessment after treatment among study group • Chi-square (× 2) test of significance was used in 2 Ultrasound No % x P value order to compare proportions between qualitative assessment parameters. Clip visualization • The confidence interval was set to 95% and the mar - Yes 55 96.5 91.525 < 0.001** gin of error accepted was set to 5%. So, the P value No 2 3.5 was considered significant as the following: Eec ff t on assessment of TTT response Yes 0 0.0 113.00 < 0.001** Table 1 Post-placement ultrasound clip assessment among No 57 100.0 study group Assessment of lesion morphology Ultrasound No % x P value Yes 0 0.0 113.00 < 0.001** assessment No 57 100.0 Clip visualization ** high significant difference Yes 57 100.0 113.000 < 0.001** No 0 0.0 Clip artifact • Probability (P value) Yes 18 31.6 31.779 < 0.001** No 39 68.5 • P value < 0.05 was considered significant. Assessment of lesion morphology • P value < 0.001 was considered as highly signifi - Yes 0 0.0 113.000 < 0.001** cant. No 57 100.0 • P value > 0.05 was considered insignificant. ** high significant difference A bdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 5 of 16 Table 3 Assessment of treatment response distribution among Our results showed that 6 patients (about 13.3%) had study group complete radiological response after NAC; in addition 2 27 patients (60%) had regressive response after the treat- Prognosis No % x P value ment (Table 3). Stationary As regards sonomamographgic assessment of breast Yes 10 22.2 11.112 0.009* clips, In 55 lesions (96.5%) the clip was easily visualized No 35 77.8 as linear hyperechoic structure compared to 2 lesions Regressive (3.5%) showed difficulty in clip visualization by ultra - Yes 27 60.0 39.778 < 0.001** sound during the follow up study after the treatment. No 18 40.0 Also our results showed that in 18 lesions (31.6%) there Progressive was clip artifact with posterior acoustic shadowing, yet Yes 2 4.4 2.002 0.157 not interfering with images interpretation or assessment No 43 95.6 of the treatment response. Radiological complete response As regards MRI, the results showed that in 45 patients Yes 6 13.3 6.340 0.012* (100%) all the surgical clips created a small signal void No 39 86.7 on MRI which was more appreciated at both T1WIs and ** high significant difference T2WIs sequences, however, the primary malignancy was easily visualized on MRI and not affecting with the image MRI Assessment 100.00% 90.00% 80.00% 70.00% 60.00% 50.00% 40.00% 30.00% 20.00% 10.00% 0.00% Best sequence to visualize the clip Fig. 3 MRI clip assessment distribution among study group Results interpretation and judgment as regards the characteriza- The study was conducted on 45 patients with a wide tion of the lesion or the pattern of enhancement (Fig. 3). age group ranging from 28 to 64 years, (mean age of As regards the complications, in only 2 patients (3.5%) 46.42 ± 9.87 years), with total number of inserted clips there was evidence of positive clip migration during the were 57 corresponding to number of lesions found in the preoperative follow up yet not interfering with the judg- total number of the patients. ment upon the tumor assessment and response to NAC. Clip signal void Effect on characterization of the lesion Effect on the pattern of enhancement T1WIs T2WIs T1WIs and T2WIs Abdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 6 of 16 surgical clips saved about 1135 Egyptian pounds equiva- Complications of clip lent to 73–75 US$ per clip (Fig. 5). 10.00% 9.00% 8.00% Discussion 7.0% 7.00% 6.00% • The study that we carried stands out the potential Pain 5.00% role of using low cost titanium surgical metallic clips Infection 3.5% 3.5% 4.00% for tumor localization in patients planned for neoad- Hematoma 3.00% junvant chemotherapy (NAC) before surgical treat- Displacement 2.00% ment. 1.00% 0.0% • Breast cancer is disease with heterogeneous etiology 0.00% associated with different characteristic histological and biological features, clinical presentations, and therapeutic responses. The most common type of Fig. 4 Complications of clips insertion distribution among study breast carcinoma is the so called invasive ductal car- group cinomas [6]. That was in agreement with our results that showed the most frequent pathological type of breast cancer seen among the studied group was IDC grade I, followed by IDC grade II and last IDC grade III (Figs. 6, 7). • NAC is considered a cornerstone step in the treat- ment of breast carcinoma especially in its early stages, as it results in decreasing the mortality inci- dence, changing the surgical approach with bet- 40000 ter surgical outcomes by conserving the breast by Surgical breast conservative surgery (BCS) or lumpectomy Commercial instead of for example modified radical mastectomy Saved / paent (MRM), convert the inoperable lesions into oper- Total Saved able ones, lessening the unfavorable postoperative complications and improving cosmetic outcomes [7]. It also assists in early detection of tumour response to therapy and tumour biology of breast Surgical CommercialSaved / Total Saved cancers [4]. paent • In one systematic review of neoadjuvant chemo- Fig. 5 Cost of surgical clips (LE) among study group therapy for operable breast cancer, patients receiving neoadjuvant chemotherapy had a lower mastectomy rate than those undergoing surgery before adjuvant Only 2 patients (3.5%) were complicated with hematoma chemotherapy [8]. immediately during the procedure as shown by ultra- • The National Cancer Comprehensive Network sound, Also 4 patients (7%) complained of Pain only guidelines recommend clip insertion before NAC, as shortly after the procedure (Fig. 4). the radiologists cannot predict the exact outcome of The study was conducted on a wide cost of surgical NAC which may be adequate enough up to complete clips for each patient ranging from 10 to 32 US$ equiv- radiological response associated with difficult identi - alent to 170 to 510 Egyptian Pounds, (mean cost of fication of the tumor site by the surgeon during sur - 13.89 ± 6.777 US$ equivalent to 215.33 ± 105.05 Egyp- gery. tian Pounds), with the average cost of the needle = 10 • As NAC has become more common, breast markers US$ (170 LE Egyptian pounds) and the clip = 1.3 US$ become more essential as it help in identification of (20 Egyptian pounds). When compared to the commer- tumor bed especially with cases with complete radio- cial breast markers with an estimated price range for logical response. Markers can be removed with the clip = 75–200 US$ (average 90 US$). So application of cancerous lesion or left in place after surgery without serious complications [9]. A bdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 7 of 16 Fig. 6 40-year-old patient with recently pathologically proven invasive ductal carcinoma (IDC) grade II, planned for neoadjuvant chemotherapy came for metallic clip placement. Breast sonomamgraphy after clip placement a1 CC View, a2 MLO view and b ultrasound images showing the surgical clip seen within the upper outer quadrant mass lesion with no significant clip artifact interfering with the image interpretation or evidence of instant complications. MRI both breasts c1 T1WIs, c2 T2WIs and c3 post contrast images done after one month of clip insertion and after start of neoadjunvant chemotherapy showing small signal void due to the clip observed in the center of the proven malignant lesion yet there was no difficulty in characterization of the lesion. After completing the course of neoadjuvant therapy, follow up sonomamography was done d1 CC views, d2 MLO view and d3 ultrasound images showing the regressive course as regards the right side upper outer breast lesion where the surgical clips are seen at the lateral end of the remaining lesion as seen on the ultrasound images where the clip seen in-place on sonomamography images which proves to be a pseudo-displacement • In Our study, we tried to use the surgical clips as sub- many types of commercial breast markers launched stitute of the commercial breast markers aiming to by different companies. Lobbes et al. [4], found that reduce the cost of this procedure. There have been cheaper surgical clips be made of safe materials as Abdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 8 of 16 Fig. 6 continued titanium, have been approved by the KFDA (Korea procedure time can be lower than those of the two- Food & Drug Administration). step clipping procedure. • In Our study, the surgical clips were inserted by • US-guided CNB technique is performed with real- needle used in the Core breast biopsy (Core needle time imaging surveillance which is considered as a biopsy CNB) by US-guided automated technique relatively safe method with few reported complica- using a commercial coaxial guiding needle. This was tions or adverse events. Therefore, the insertion pro - in agreement with Hassan et al. [2], who used dispos- cess itself is not considered an onerous duty by breast able Guillotine biopsy needle 16G x 20 cm GTA radiologists [1]. with the similar automated technique that is similar • Our study was based on the hypothesis that radio- to the core breast biopsy technique that is considered paque markers can replace commercial breast mark- a safe easy procedure done completely under real- ers for tumor localization as well as for the assess- time ultrasound surveillance to identify the desired ment of tumor response after NAC, yet without location for the surgical clips with an estimated time interfering with radiologic multimodality evaluation of the whole procedure about 6–10 min. including sono-mammography and MRI, with no • The surgical breast marker can be placed at the significant complications and with lower cost. That (CNB) performed site where there is no tissue injury what was illustrated as follows. due to repeated insertion and less bleeding with • As regards the complications of the clip; the migra- lower probability of tumor cell seeding. Kaufmann tion of surgical clips and related complications can be et al. [9], found that on performing on-site clipping a limitation of surgical clip insertion. Clip migration immediately after CNB both the medical costs and may occur immediately after biopsy or may be seen on later follow-up sono-mammograms [1]. A bdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 9 of 16 Fig. 6 continued Abdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 10 of 16 Fig. 7 37-year-old patient with left breast lump, recently pathologically proven invasive ductal carcinoma (IDC) grade II came for clip insertion before the start of chemotherapy, Breast sonomamography after clip placement a1 CC view, a2 MLO view and b1 ultrasound images showing the surgical clip seen within the left breast lobulated hypoechoic mass (b2) with an adjacent smaller satellite lesion with a clip seen inside, yet both clips show no artifact interfering with images interpretation. MRI of both breasts c1 T1WIs first clip inside lesion c2 T1WIs second clip and c3 post contrast) done showing a signal void of two metallic surgical clips seen at UOQ, still seen inside two left sided ill-defined speculated malignant mass lesions showing evidence of post contrast enhancement. After completing the course of neoadjuvant therapy, follow up sonomamography was done d1 and d2 shows two surgical clips still noted in left breast solid masses showing regressive course as regards the size with the clips still seen in the same site compared to the previous studies • In our study only 2 patients (3.5%) showed radio- there was no change in the clip distance measured at logical evidence of clip displacement where there the mammography images on three different quad - were > 1 cm difference between the distance of the rants (distance from skin, from areola and from chest clip at the pretreatment sonomamography and fol- wall), only the displacement was noted on ultrasound low up sono-mammography after NAC, yet not images, which confirms that the clip did not move, interfering with image interpretation. Those results but the primary lesion changed in size in relation to were close to Hassan et al. [2] study, who used US the clip. guided inserted surgical clips followed by follow up • That was explained by Lee et al. [10] who found sono-mammography after treatment, and reported that the cause of clip migration is the change of the two cases representing about 6.25% with positive clip size and shape of the tumor in which the clip was migration. deployed after NAC or radiotherapy, which may be • In our study, from the cases that showed regressive misinterpreted as clip migration. course regarding the size of the lesion, two cases had • Our result wasn’t in agreement with Hassan et al. evidence of clip displacement. In those two cases [2], and Margolin et al. [11] who explained the A bdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 11 of 16 Fig. 7 continued Abdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 12 of 16 cause of the clip migration due to predominant ment with Young et al. [1] who found 100% of the fatty elements of the breast tissue ACR (a) which inserted clips appeared as linear hyperechoic struc- may cause redundant breast tissue and low tissue tures on the ultrasound. resistance. But the point of disagreement was that • That also stands with Koo et al. [13], who compared the two cases in our study with positive migration between the surgical clips and commercial breast had a heterogeneous breast tissue categorized as markers found that marker visibility was little more ACR (c), which couldn’t explain the cause of dis- common when using Liga Clip (surgical clips) (about placement in our study. 91.1%, 51 of 56) than when using Cormark mark- • There are different breast cancer types, but the ers (commercial clips) (about 86.9%, 53 of 61) in all most common type of breast carcinoma is so called cases. And in cases where no residual lesion could be invasive ductal carcinomas and in most of the cases noted on US during the follow up after NAC, marker breast cancer appears as solid irregular or specu- visibility was more common when using LigaClip lated lesions with some lesions may show areas of markers (88.2%, 15 of 17) than when using Cormark cystic degeneration or necrosis. The variations in markers (80% 8 of 10). breast density, tumor composition as solid with or • The two cases in which there was difficulty in clip without or cystic degeneration or necrosis and con- visualization showed complete radiological response. sequently the tissue resistance was seen to be a fac- Won et al. [14] explained the previous findings on tor affecting the degree of clip migration. The low the hypothesis that the hyperechoic (metallic) clip tissue resistance as in fatty breasts may allow clips can be easily visible against the background of the to easily migrate by interfering with the fixation of hypoechoic nature of the tumor. When the tumors surgical clips especially after decrease in the size of becomes smaller and even disappear as NAC pro- the mass which is an important factor for clip fixa - ceeds this hinders differentiating the clip from the tion and stability. background of the echogenic fat strands. • Previous studies on clip migration as Hassan et al. • Also our results showed that 18 lesions (31.6%) [2], and Margolin et al. [11] have shown that clips showed clip Artifact with posterior acoustic shad- move more easily in fatty breast tissue; however, owing while 39 lesions (68.4%) showed no Clip arti- Carolyn et al. [12] showed that some of this appar- fact that was not in agreement with Hassan et al. [2]. ent migration may be also due to the greater pliabil- study which recoded only 3 patients (9.4%) with clip ity and mobility of the fatty breast. However, clips artifact. are generally inserted into the center of the mass or • In our study this clip artifact did not interfere with the most solid component with higher tissue resist- ultrasound assessment of the lesion, where in 45 ance because of its solid nature. Thus, the chance of patients (100%) the clip neither interfere in assess- clip migration should be lower. ment of the treatment response nor the morphology • Results also shows that, there were only 2 patients of the lesion by sono-mammography. That agrees (about 3.5%) had hematoma during the procedure as with Young et al. [1], and other multiple previous shown by ultrasound, and only 4 patients (7%) com- studies which show that application of surgical clips plained of pain shortly after the procedure. even in the presence of artifact won’t interfere with • Our results revealed that the rest of the patients had neither sonographic assessment of the lesion nor no evidence of pain or heat sensation either during the size of the lesion and therefore assessment of the the procedure or during MRI, also the rest of the treatment response. study population showed no evidence of hematoma • As regards MRI assessment of the clip: Breast metal- formation or infection. All the above data confirms lic clips can cause artifacts on MRI, depending on that the clip insertion is highly significant compli - magnetic susceptibility, clip quality, size, shape, ori- cation-free procedure, that was agreed with Young entation, position, and used MRI parameters [1]. et al. [1], who showed no significant complications • In our study, in all our patients (100%) the surgical along the studied group clips created a small signal void on MRI; however, the • As regards sono-mammographgic assessment of the primary lesion was easily visualized on MRI and did clip, our study shows that: from the total number not interfere with the image interpretation and judg- of inserted clips, 55 clips (96.5%) were easily visual- ment as regards the characterization of the lesion or ized as linear hyperechoic structures compared to the enhancement pattern. 2 clips (3.5%) showed difficulty in visualization by • The inserted clips appeared on MRI as small signal Ultrasound that was noted during the follow up voids due to its paramagnetic or susceptibility prop- after receiving NAC. These results were in-agree - erties, which is more appreciated at both T1WIs and A bdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 13 of 16 T2WIs, where in 15 patients (26.3%) the clips were • That emphasizes the role of clips insertion for local - best visualized at T1WIs, 8 patients (14%) at T2WIs izing the site of the lesion especially in cases show- compared to 34 patients (59.6%) where the clips were ing improving disease response that may interfere best visualized at both T1WIs and T2WIs images, in radiological recognition of the site of the lesions this can be explained as T1 sequences are performed and the tumor bed. Where in our study about 33 without fat saturation which allow metal markers patients (about 73%) showed improving disease to be better detected, this detection is based on the response including patients achieving a complete or magnetic susceptibility artifact best seen on T1 gra- near-complete response to NAC. In this situation clip dient-echo sequences, created by the metallic nature insertion effectively addresses the problem of preop - of the marker. The longer the TE of the sequence the erative localization of the tumor and if the clip was more this artifact is visible so T1 sequence was found not inserted the tumor bed, those patients could have to be best sequence for detection metallic artifact of been lost and the surgeons would have to undergo the clip [15] (Fig. 8). major surgical excision as Modified radical mastec - • As regards assessment of prognosis of treatment tomy (MRM) instead of conservative breast surger- response; the assessment of tumor response to NAC ies. as confirmed on US, mammography, and MRI is • As regards the Cost of the clip: The study was con - important and done according to RECIST criteria, ducted on a wide cost of surgical clips with the aver- Response evaluation criteria in solid tumors refers age cost of the needle = 10US$ equivalent to 170 to a set of published rules used to assess tumor bur- LE Egyptian pounds and the single clip = 1.3 US$ den in order to provide an objective assessment of equivalent to 20 Egyptian pounds with total cost per response to therapy. The RECIST criteria can be used patient (170 + 20 = 190) about 190 Egyptian Pounds with CT, MRI or conventional radiography (in some equivalent to 12–13 US$, compared to Hassan et al. instances) [15]. [2], study that revealed that the average cost of the • Tumor response to neoadjuvant chemotherapy may single surgical clip was 145 ± 20 LE Egyptian pounds be either complete response (CR) with disappear- which is almost equivalent to8–9US$. This was in ance of all lesions, partial response (PR)/regressive agreement to Masroor et al. [17] study who found response where > 30% decrease in sum of all tar- that the cost of surgical clips was about 9 US$, and get lesions in longest axis measurement, stable dis- similar to the study done in South Korea since 2015 ease (SD) and progressive disease (PD) according to where the calculated cost was 10 US$ per clip [1]. RECIST criteria [17]. • This is of much low cost when compared to the • Clearly, the ideal result for a patient undergoing neo- commercial breast markers with an estimated price adjuvant chemotherapy is eradication of the malig- range for clip = 75–200 US$ internationally (aver- nant disease in the breast and in the axillary lymph age 90 US$). nodes (pCR). • This means that the use of surgical clips saved about • In our study, there were 6 patients (about 13.3%) had 75–76 US$ which is equivalent to 1135 Egyptian radiological complete response after NAC, com- pounds that was close to Hassan et al. [2], which pared to Hassan et al. [2], study where they found 14 recorded the saved price about 80–82 US$ for each patients (about 43.75%) showed complete pathologi- clip, this confirms that surgical clips of the highly cal response and that was close to Edeiken et al. [16] considerable low cost compared to the commercial study which found 47% of the study population had breast markers. complete response. • Also in our study there were 27 patients (60%) showed regressive course after NAC while only 10 Conclusion patients (22.2%) had stationary course regarding the Our study proved that the use of breast markers is size of the lesions, and only 2 cases (4.4%) showed mandatory before NAC where sonographically-guided progressive disease response with highly signifi - metallic surgical clips can safely substitute the com- cant difference between the studied group showing mercial tissue markers as tumor localization. Surgical improving disease response and the other studied clips are effective, considerable and safe for the patient, groups. easily visualized on imaging, do not interfere with • In two patients out of 27 patients who had regressive assessment of treatment response, with no evidence of course, the lesions were not palpable by the surgeons complications and are of low cost compared with the and needed preoperative wire localization. commercial breast clips. Abdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 14 of 16 Fig. 8 42-year-old patient with breast lump and axillary masses, the patient came for tru-cut biopsy, which shows advanced breast carcinoma, planned for neoadjuvant chemotherapy and metallic clip placement. The patient received first cycle chemotherapy and came for clip insertion, Breast sonomamography after clip placement a CC view and b ultrasound images showing the metallic clip seen inside the upper outer quadrant mass lesion with no artifact or posterior acoustic shadowing hindering proper visualization of the lesion. MRI of both breasts done after other cycle of NAC c1 T1WIs, c2 T2WIs, c3 post contrast images and c4 subtracted post contrast images) showing the signal void of the inserted surgical clip inside the previously noted breast lesion, with no difficulty in characterization of the lesion. After completing the course of neoadjuvant therapy, follow up sonomamography was done d1 ultrasound image and d2 MLO view showing the surgical clips still seen at the left breast irregular mass lesion which shows appreciable regressive course as regards the size with the clip still seen in the same site compared to the previous studies e ultrasound image shows preoperative wire localization guided by the previously inserted surgical clip due to appreciable regressive course of the size of the lesion A bdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 15 of 16 Fig. 8 continued Limitations Recommendations • In our study group, The most common type of • For further multi-parametric studies, we recom- breast carcinoma was invasive ductal carcinomas, mend applying the one step clipping procedure and with most of the lesions were solid and no com- to place the surgical clip at the same setting of the plex cystic lesions nor any cystic degeneration were core tissue biopsy to avoid repeating insertion of detected, which made us unable to precisely study the needle, minimize tissue injury, decrease inci- the effect of the tissue resistance and nature on the dence of tumor cell seedling and to lower the cost radiological assessment of the clip and detection and the procedure time. rate of clip migration. • Also, other studies are needed to study this tech- • Relatively small sample size, and that was due to nique over larger number of patients to detect the high cost of MRI and presence of some contraindi- rate clip migration on other lesions with different cation in some patients. histological types and different tissue natures. Abdelfatah et al. Egypt J Radiol Nucl Med (2022) 53:71 Page 16 of 16 Abbreviations and future of neoadjuvant systemic therapy in primary breast cancer. NAC: Neoadjuvant chemotherapy; MRI: Magnetic resonance imaging.; pCR: Ann Surg Oncol 19(1508–16):8 Pathological complete response; rCR: Radiological complete response; GFR: 10. Lee SG, Piccoli CW, Hughes JS (2001) Displacement of microcalcifications Glomerular filtration rate; CNB: Core needle biopsy; RECIST: Response evalua- during stereotactic 11-gaugedirectional vacuum-assisted biopsy with tion criteria in solid tumors. marking clip placement: case report. Radiology 219(495–497):10 11. Margolin FR, Kaufman L, Denny SR et al (2003) Metallic marker placement Acknowledgements after stereotactic core biopsy of breast calcifications: comparison of two The author thanks all the study participants for their patience and support. clips and deployment techniques. Am J Roentgenol 181:1685–1690 12. Carolyn RM, Meredith AK, Chris JDM et al (2015) Radiographer technique: Authors’ contributions does it contribute to the question of clip migration? J Med Imaging NOS: collected and analyzed the data, wrote the manuscript, prepared the Radiat Oncol 59:564–570 cases, performed required interval procedure, measurements and statistical 13. Koo JH, Eun-Kyung K, Hee JM, Jung HY, Vivian YP, Min JK (2019) Com- analysis, and prepared figures and tables. SFI: suggested the research idea, parison of breast tissue markers for tumor localization in breast cancer shared in data collection and analysis, reviewed literature, statistical analysis, patients undergoing neoadjuvant chemotherapy. Ultrasonography and manuscript editing. AIH: reviewed the manuscript and statistical analysis. 38(4):336–344. https:// doi. org/ 10. 14366/ usg. 19004 RHA: reviewed the manuscript and statistical analysis. All authors read and 14. Hk W, Hye JK, See HK et al (2019) Ultrasound-guided dual-localization approved the final manuscript. for axillary nodes before and after neoadjuvant chemotherapy with clip and activated charcoal in breast cancer patients: a feasibility study. BMC Funding Cancer 19:859. https:// doi. org/ 10. 1186/ s12885- 019- 6095-1 This study had no funding from any resource. 15. Orlacchio A, Bolacchi F, Rotili A et al (2008) MR breast imaging: a com- parative analysis of conventional and parallel imaging acquisition. Radiol Availability of data and materials Med 113:465–476 The datasets used and analyzed during the current study are available from 16. Edeiken BS, Fornage BD, Bedi DG et al (1999) US-guided implantation of the corresponding author on reasonable request. metallic markers for permanent localization of the tumor bed in patients with breast cancer who undergo preoperative chemotherapy. Radiology 213:895–900 Declarations 17. Masroor I, Zeeshan S, Afzal S et al (2016) Outcome and cost-effectiveness of ultrasonographically guided surgical clip placement for tumor localiza- Ethics approval and consent to participate tion in patients undergoing neoadjuvant chemotherapy for breast This study was approved by the Research Ethics Committee of the Faculty of cancer. Asian Pac J Cancer Prev 16(18):8339–8343 Medicine at Ain Shams University in Egypt in March 2020; Reference number of approval: MD87/2020. Publisher’s Note Consent for publication Springer Nature remains neutral with regard to jurisdictional claims in pub- All patients included in this research gave written informed consent to publish lished maps and institutional affiliations. the data contained within this study. Competing interests The authors declare that they have no competing interests. Received: 2 November 2021 Accepted: 2 March 2022 References 1. 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Ellis P, Schnitt SJ, Sastre-Garau X et al (2003) Invasive breast carcinoma. In: Tavassoli FA, Devilee P (eds) WHO classification of tumours pathology and genetics of tumours of the breast and female genital organs. IARC Press 7. Kim Z, Min SY, Yoon CS, Lee HJ et al (2014) The basic facts of Korean breast cancer in 2011: results of a nationwide survey and breast cancer registry database. J Breast Cancer 17:99–106 8. Mieog JSD, van der Hage J, van de Velde CJH (2007) Neoadjuvant chemo- therapy for opérable breast cancer. Br J Surg 94:1198–1200 9. Kaufmann M, von Minckwitz G, Mamounas EP et al (2012) Recommenda- tions from an international consensus conference on the current status
Egyptian Journal of Radiology and Nuclear Medicine – Springer Journals
Published: Mar 16, 2022
Keywords: Breast cancer; Neoadjunvant chemotherapy; Surgical clips
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