Publications by authors named "Theo J M Ruers"

81 Publications

Imaging PPG for In Vivo Human Tissue Perfusion Assessment during Surgery.

J Imaging 2022 Mar 31;8(4). Epub 2022 Mar 31.

IGT & US Devices & Systems, Philips Research, High Tech, Campus 34, 5656 AE Eindhoven, The Netherlands.

Surgical excision is the golden standard for treatment of intestinal tumors. In this surgical procedure, inadequate perfusion of the anastomosis can lead to postoperative complications, such as anastomotic leakages. Imaging photoplethysmography (iPPG) can potentially provide objective and real-time feedback of the perfusion status of tissues. This feasibility study aims to evaluate an iPPG acquisition system during intestinal surgeries to detect the perfusion levels of the microvasculature tissue bed in different perfusion conditions. This feasibility study assesses three patients that underwent resection of a portion of the small intestine. Data was acquired from fully perfused, non-perfused and anastomosis parts of the intestine during different phases of the surgical procedure. Strategies for limiting motion and noise during acquisition were implemented. iPPG perfusion maps were successfully extracted from the intestine microvasculature, demonstrating that iPPG can be successfully used for detecting perturbations and perfusion changes in intestinal tissues during surgery. This study provides proof of concept for iPPG to detect changes in organ perfusion levels.
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http://dx.doi.org/10.3390/jimaging8040094DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9031653PMC
March 2022

Layer thickness prediction and tissue classification in two-layered tissue structures using diffuse reflectance spectroscopy.

Sci Rep 2022 02 1;12(1):1698. Epub 2022 Feb 1.

Department of Surgery, Netherlands Cancer Institute, 1066 CX, Amsterdam, The Netherlands.

During oncological surgery, it can be challenging to identify the tumor and establish adequate resection margins. This study proposes a new two-layer approach in which diffuse reflectance spectroscopy (DRS) is used to predict the top layer thickness and classify the layers in two-layered phantom and animal tissue. Using wavelet-based and peak-based DRS spectral features, the proposed method could predict the top layer thickness with an accuracy of up to 0.35 mm. In addition, the tissue types of the first and second layers were classified with an accuracy of 0.95 and 0.99. Distinguishing multiple tissue layers during spectral analyses results in a better understanding of more complex tissue structures encountered in surgical practice.
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http://dx.doi.org/10.1038/s41598-022-05751-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8807816PMC
February 2022

Nationwide registry study on trends in localization techniques and reoperation rates in non-palpable ductal carcinoma in situ and invasive breast cancer.

Br J Surg 2021 12;109(1):53-60

Department of Surgical Oncology, Netherlands Cancer Institute, Amsterdam, The Netherlands.

Background: There is a transition from wire-guided localization (WGL) of non-palpable breast cancer to other localization techniques. Multiple prospective studies have sought to establish superior clinical outcomes for radioactive-seed localization (RSL), but consistent and congruent evidence is missing.

Methods: In this study, female patients with breast cancer operated with breast-conserving surgery after tumour localization of a non-palpable breast cancer or ductal carcinoma in situ (DCIS) were included. The cohort was identified from the nationwide Netherlands Breast Cancer Audit conducted between 2013 and 2018. Trends in localization techniques were analysed. Univariable and multivariable analyses were performed to assess the association between the localization technique and the probability of a reoperation.

Results: A total of 28 370 patients were included in the study cohort. The use of RSL increased from 15.7 to 61.1 per cent during the study years, while WGL decreased from 75.4 to 31.6 per cent. The localization technique used (RSL versus WGL) was not significantly associated with the odds of a reoperation, regardless of whether the lesion was DCIS (odds ratio 0.96 (95 per cent c.i. 0.89 to 1.03; P = 0.281)) or invasive breast cancer (OR 1.02 (95 per cent c.i. 0.96 to 1.10; P = 0.518)).

Conclusion: RSL is rapidly replacing WGL as the preoperative localization technique in breast surgery. This large nationwide registry study found no association between the type of localization technique and the odds of having a reoperation, thus confirming the results of previous prospective cohort studies.
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http://dx.doi.org/10.1093/bjs/znab339DOI Listing
December 2021

Surgical navigation for challenging recurrent or pretreated intra-abdominal and pelvic soft tissue sarcomas.

J Surg Oncol 2021 Dec 28;124(7):1173-1181. Epub 2021 Jul 28.

Department of Surgical Oncology, The Netherlands Cancer Institute/Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.

Background: This study assessed whether electromagnetic navigation can be of added value during resection of recurrent or post-therapy intra-abdominal/pelvic soft tissue sarcomas (STS) in challenging locations.

Materials And Methods: Patients were included in a prospective navigation study. A pre-operatively 3D roadmap was made and tracked using electromagnetic reference markers. During the operation, an electromagnetic pointer was used for the localization of the tumor/critical anatomical structures. The primary endpoint was feasibility, secondary outcomes were safety and usability.

Results: Nine patients with a total of 12 tumors were included, 7 patients with locally recurrent sarcoma. Three patients received neoadjuvant radiotherapy and three other patients received neoadjuvant systemic treatment. The median tumor size was 4.6 cm (2.4-10.4). The majority of distances from tumor to critical anatomical structures was <0.5 cm. The tumors were localized using the navigation system without technical or safety issues. Despite the challenging nature of these resections, 89% were R0 resections, with a median blood loss of 100 ml (20-1050) and one incident of vascular damage. Based on the survey, surgeons stated navigation resulted in shorter surgery time and made the resections easier.

Conclusion: Electromagnetic navigation facilitates resections of challenging lower intra-abdominal/pelvic STS and might be of added value.
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http://dx.doi.org/10.1002/jso.26624DOI Listing
December 2021

Technical note: Validation of 3D ultrasound for image registration during oncological liver surgery.

Med Phys 2021 Oct 29;48(10):5694-5701. Epub 2021 Jul 29.

Department of Surgical Oncology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek, Amsterdam, The Netherlands.

Purpose: Registration of pre- and intraoperative images is a crucial step of surgical liver navigation, where rigid registration of vessel centerlines is currently commonly used. When using 3D ultrasound (US), accuracy during navigation might be influenced by the size of the intraoperative US volume, yet the relationship between registration accuracy and US volume size is understudied. In this study, we specify an optimal 3D US volume size for registration using varying volumes of liver vasculature. While previous studies measured accuracy at registered fiducials, in this work, accuracy is determined at the target lesion which is clinically the most relevant structure.

Methods: Three-dimensional US volumes were acquired in 14 patients after laparotomy and liver mobilization. Manual segmentation of vasculature and centerline extraction was performed. Intraoperative and preoperative vasculature centerlines were registered with coherent point drift, using different sub-volumes (sphere with radius r = 30, 40, …, 120 mm). Accuracy was measured by fiducial registration error (FRE) between vessel centerlines and target registration error (TRE) at the center of the target lesion.

Results: The lowest FRE for vessel registration was reached with r = 50 mm (6.5 ± 2.5 mm), the highest with r = 120 mm (7.1 ± 2.1 mm). Clinical accuracy at the target lesion, resulted most accurate (TRE = 8.8 ± 5.0 mm) in sub-volumes with a radius of 50 mm. Smaller US sub-volumes resulted in lower average TREs when compared to larger US sub-volumes (Pearson's correlation coefficient R = 0.91, p < 0.001).

Conclusion: Our results indicate that there is a linear correlation between US volume size and registration accuracy at the tumor. Volumes with radii of 50 mm around the target lesion yield higher accuracy (p < 0.05) (Trial number IRBd18032, 11 September 2018).
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http://dx.doi.org/10.1002/mp.15080DOI Listing
October 2021

Randomized controlled trial comparing magnetic marker localization (MaMaLoc) with wire-guided localization in the treatment of early-stage breast cancer.

Breast J 2021 08 17;27(8):638-650. Epub 2021 Jun 17.

Department of Surgery, Franciscus Gasthuis and Vlietland, Rotterdam, The Netherlands.

Wire-guided localization (WGL) is the standard of care in the surgical treatment of nonpalpable breast tumors. In this study, we compare the use of a new magnetic marker localization (MaMaLoc) technique to WGL in the treatment of early-stage breast cancer patients. Open-label, single-center, randomized controlled trial comparing MaMaLoc (intervention) to WGL (control) in women with early-stage breast cancer. Primary outcome was surgical usability measured using the System Usability Scale (SUS, 0-100 score). Secondary outcomes were patient reported, clinical, and pathological outcomes such as retrieval rate, operative time, resected specimen weight, margin status, and reoperation rate. Thirty-two patients were analyzed in the MaMaLoc group and 35 in the WGL group. Patient and tumor characteristics were comparable between groups. No in situ complications occurred. Retrieval rate was 100% in both groups. Surgical usability was higher for MaMaLoc: 70.2 ± 8.9 vs. 58.1 ± 9.1, p < 0.001. Patients reported higher overall satisfaction with MaMaLoc (median score 5/5) versus WGL (score 4/5), p < 0.001. The use of magnetic marker localization (MaMaLoc) for early-stage breast cancer is effective and has higher surgical usability than standard WGL.
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http://dx.doi.org/10.1111/tbj.14262DOI Listing
August 2021

Optical tissue measurements of invasive carcinoma and ductal carcinoma in situ for surgical guidance.

Breast Cancer Res 2021 05 22;23(1):59. Epub 2021 May 22.

Department of Surgery, Netherlands Cancer Institute-Antoni van Leeuwenhoek Hospital, Postbus 90203, 1006, Amsterdam, BE, Netherlands.

Background: Although the incidence of positive resection margins in breast-conserving surgery has decreased, both incomplete resection and unnecessary large resections still occur. This is especially the case in the surgical treatment of ductal carcinoma in situ (DCIS). Diffuse reflectance spectroscopy (DRS), an optical technology based on light tissue interactions, can potentially characterize tissue during surgery thereby guiding the surgeon intraoperatively. DRS has shown to be able to discriminate pure healthy breast tissue from pure invasive carcinoma (IC) but limited research has been done on (1) the actual optical characteristics of DCIS and (2) the ability of DRS to characterize measurements that are a mixture of tissue types.

Methods: In this study, DRS spectra were acquired from 107 breast specimens from 107 patients with proven IC and/or DCIS (1488 measurement locations). With a generalized estimating equation model, the differences between the DRS spectra of locations with DCIS and IC and only healthy tissue were compared to see if there were significant differences between these spectra. Subsequently, different classification models were developed to be able to predict if the DRS spectrum of a measurement location represented a measurement location with "healthy" or "malignant" tissue. In the development and testing of the models, different definitions for "healthy" and "malignant" were used. This allowed varying the level of homogeneity in the train and test data.

Results: It was found that the optical characteristics of IC and DCIS were similar. Regarding the classification of tissue with a mixture of tissue types, it was found that using mixed measurement locations in the development of the classification models did not tremendously improve the accuracy of the classification of other measurement locations with a mixture of tissue types. The evaluated classification models were able to classify measurement locations with > 5% malignant cells with a Matthews correlation coefficient of 0.41 or 0.40. Some models showed better sensitivity whereas others had better specificity.

Conclusion: The results suggest that DRS has the potential to detect malignant tissue, including DCIS, in healthy breast tissue and could thus be helpful for surgical guidance.
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http://dx.doi.org/10.1186/s13058-021-01436-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8141169PMC
May 2021

Clinical Implementation of In-House Developed MR-Based Patient-Specific 3D Models of Liver Anatomy.

Eur Surg Res 2020 28;61(4-5):143-152. Epub 2021 Jan 28.

Department of Surgical Oncology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Amsterdam, The Netherlands.

Knowledge of patient-specific liver anatomy is key to patient safety during major hepatobiliary surgery. Three-dimensional (3D) models of patient-specific liver anatomy based on diagnostic MRI images can provide essential vascular and biliary anatomical insight during surgery. However, a method for generating these is not yet publicly available. This paper describes how these 3D models of the liver can be generated using open source software, and then subsequently integrated into a sterile surgical environment. The most common image quality aspects that degrade the quality of the 3D models as well possible ways of eliminating these are also discussed. Per patient, a single diagnostic multiphase MRI scan with hepatospecific contrast agent was used for automated segmentation of liver contour, arterial, portal, and venous anatomy, and the biliary tree. Subsequently, lesions were delineated manually. The resulting interactive 3D model could be accessed during surgery on a sterile covered tablet. Up to now, such models have been used in 335 surgical procedures. Their use simplified the surgical treatment of patients with a high number of liver metastases and contributed to the localization of vanished lesions in cases of a radiological complete response to neoadjuvant treatment. They facilitated perioperative verification of the relationship of tumors and the surrounding vascular and biliary anatomy, and eased decision-making before and during surgery.
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http://dx.doi.org/10.1159/000513335DOI Listing
October 2021

Tongue Tumor Detection in Hyperspectral Images Using Deep Learning Semantic Segmentation.

IEEE Trans Biomed Eng 2021 04 18;68(4):1330-1340. Epub 2021 Mar 18.

Objective: The utilization of hyperspectral imaging (HSI) in real-time tumor segmentation during a surgery have recently received much attention, but it remains a very challenging task.

Methods: In this work, we propose semantic segmentation methods, and compare them with other relevant deep learning algorithms for tongue tumor segmentation. To the best of our knowledge, this is the first work using deep learning semantic segmentation for tumor detection in HSI data using channel selection, and accounting for more spatial tissue context, and global comparison between the prediction map, and the annotation per sample. Results, and Conclusion: On a clinical data set with tongue squamous cell carcinoma, our best method obtains very strong results of average dice coefficient, and area under the ROC-curve of [Formula: see text], and [Formula: see text], respectively on the original spatial image size. The results show that a very good performance can be achieved even with a limited amount of data. We demonstrate that important information regarding tumor decision is encoded in various channels, but some channel selection, and filtering is beneficial over the full spectra. Moreover, we use both visual (VIS), and near-infrared (NIR) spectrum, rather than commonly used only VIS spectrum; although VIS spectrum is generally of higher significance, we demonstrate NIR spectrum is crucial for tumor capturing in some cases.

Significance: The HSI technology augmented with accurate deep learning algorithms has a huge potential to be a promising alternative to digital pathology or a doctors' supportive tool in real-time surgeries.
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http://dx.doi.org/10.1109/TBME.2020.3026683DOI Listing
April 2021

Nonlinear multispectral imaging for tumor delineation.

J Biomed Opt 2020 09;25(9)

University of Twente, Faculty of Science and Technology, Enschede, Netherlands.

Significance: In breast-preserving tumor surgery, the inspection of the excised tissue boundaries for tumor residue is too slow to provide feedback during the surgery. The discovery of positive margins requires a new surgery which is difficult and associated with low success. If the re-excision could be done immediately this is believed to improve the success rate considerably.

Aim: Our aim is for a fast microscopic analysis that can be done directly on the excised tissue in or near the operating theatre.

Approach: We demonstrate the combination of three nonlinear imaging techniques at selected wavelengths to delineate tumor boundaries. We use hyperspectral coherent anti-Stokes Raman scattering (CARS), second harmonic generation (SHG), and two-photon excited fluorescence (TPF) on excised patient tissue.

Results: We show the discriminatory power of each of the signals and demonstrate a sensitivity of 0.87 and a specificity of 0.95 using four CARS wavelengths in combination with SHG and TPF. We verify that the information is independent of sample treatment.

Conclusions: Nonlinear multispectral imaging can be used to accurately determine tumor boundaries. This demonstration using microscopy in the epi-direction directly on thick tissue slices brings this technology one step closer to clinical implementation.
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http://dx.doi.org/10.1117/1.JBO.25.9.096001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7470215PMC
September 2020

Understanding the Costs of Surgery: A Bottom-Up Cost Analysis of Both a Hybrid Operating Room and Conventional Operating Room.

Int J Health Policy Manag 2022 Mar 1;11(3):299-307. Epub 2022 Mar 1.

Department of Operating Rooms, Radboud Institute for Health Sciences, Radboud University Medical Center, Nijmegen, The Netherlands.

Background: Over the past decade, many hospitals have adopted hybrid operating rooms (ORs). As resources are limited, these ORs have to prove themselves in adding value. Current estimations on standard OR costs show great variety, while cost analyses of hybrid ORs are lacking. Therefore, this study aims to identify the cost drivers of a conventional and hybrid OR and take a first step in evaluating the added value of the hybrid OR.

Methods: A comprehensive bottom-up cost analysis was conducted in five Dutch hospitals taking into account: construction, inventory, personnel and overhead costs by means of interviews and hospital specific data. The costs per minute for both ORs were calculated using the utilization rates of the ORs. Cost drivers were identified by sensitivity analyses.

Results: The costs per minute for the conventional OR and the hybrid OR were €9.45 (€8.60-€10.23) and €19.88 (€16.10- €23.07), respectively. Total personnel and total inventory costs had most impact on the conventional OR costs. For the hybrid OR the costs were mostly driven by utilization rate, total inventory and construction costs. The results were incorporated in an open access calculation model to enable adjustment of the input parameters to a specific hospital or country setting.

Conclusion: This study estimated a cost of €9.45 (€8.60-€10.23) and €19.88 (€16.10-€23.07) for the conventional and hybrid OR, respectively. The main factors influencing the OR costs are: total inventory costs, total construction costs, utilization rate, and total personnel costs. Our analysis can be used as a basis for future research focusing on evaluating value for money of this promising innovative OR. Furthermore, our results can inform surgeons, and decision and policy-makers in hospitals on the adoption and optimal utilization of new (hybrid) ORs.
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http://dx.doi.org/10.34172/ijhpm.2020.119DOI Listing
March 2022

Association of Image-Guided Navigation With Complete Resection Rate in Patients With Locally Advanced Primary and Recurrent Rectal Cancer: A Nonrandomized Controlled Trial.

JAMA Netw Open 2020 07 1;3(7):e208522. Epub 2020 Jul 1.

Department of Surgical Oncology, the Netherlands Cancer Institute-Antoni van Leeuwenhoek, Amsterdam, the Netherlands.

Importance: The percentage of tumor-positive surgical resection margin rates in patients treated for locally advanced primary or recurrent rectal cancer is high. Image-guided navigation may improve complete resection rates.

Objective: To ascertain whether image-guided navigation during rectal cancer resection improves complete resection rates compared with surgical procedures without navigation.

Design, Setting, And Participants: This prospective single-center nonrandomized controlled trial was conducted at the Netherlands Cancer Institute-Antoni van Leeuwenhoek in Amsterdam, the Netherlands. The prospective or navigation cohort included adult patients with locally advanced primary or recurrent rectal cancer who underwent resection with image-guided navigation between February 1, 2016, and September 30, 2019, at the tertiary referral hospital. Clinical results of this cohort were compared with results of the historical cohort, which was composed of adult patients who received rectal cancer resection without image-guided navigation between January 1, 2009, and December 31, 2015.

Intervention: Rectal cancer resection with image-guided navigation.

Main Outcomes And Measures: The primary end point was the complete resection rate, measured by the amount of tumor-negative resection margin rates. Secondary outcomes were safety and usability of the system. Safety was evaluated by the number of navigation system-associated surgical adverse events. Usability was assessed from responses to a questionnaire completed by the participating surgeons after each procedure.

Results: In total, 33 patients with locally advanced or recurrent rectal cancer were included (23 men [69.7%]; median [interquartile range] age at start of treatment, 61 [55.0-69.0] years). With image-guided navigation, a radical resection (R0) was achieved in 13 of 14 patients (92.9%; 95% CI, 66.1%-99.8%) after primary resection of locally advanced tumors and in 15 of 19 patients (78.9%; 95% CI, 54.4%-94.0%) after resection of recurrent rectal cancer. No navigation system-associated complications occurred before or during surgical procedures. In the historical cohort, 142 patients who underwent resection without image-guided navigation were included (95 men [66.9%]; median [interquartile range] age at start of treatment, 64 [55.0-70.0] years). In these patients, an R0 resection was accomplished in 85 of 101 patients (84.2%) with locally advanced rectal cancer and in 20 of 41 patients (48.8%) with recurrent rectal cancer. A significant difference was found between the navigation and historical cohorts after recurrent rectal cancer resection (21.1% vs 51.2%; P = .047). For locally advanced primary tumor resection, the difference was not significant (7.1% vs 15.8%; P = .69). Surgeons stated in completed questionnaires that the navigation system improved decisiveness and helped with tumor localization.

Conclusions And Relevance: Findings of this study suggest that image-guided navigation used during rectal cancer resection is safe and intuitive and may improve tumor-free resection margin rates in recurrent rectal cancer.

Trial Registration: Netherlands Trial Register Identifier: NTR7184.
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http://dx.doi.org/10.1001/jamanetworkopen.2020.8522DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7344384PMC
July 2020

Accurate surgical navigation with real-time tumor tracking in cancer surgery.

NPJ Precis Oncol 2020 8;4. Epub 2020 Apr 8.

1Department of Surgical Oncology, The Netherlands Cancer Institute, Amsterdam, The Netherlands.

In the past decades, image-guided surgery has evolved rapidly. In procedures with a relatively fixed target area, like neurosurgery and orthopedics, this has led to improved patient outcomes. In cancer surgery, intraoperative guidance could be of great benefit to secure radical resection margins since residual disease is associated with local recurrence and poor survival. However, most tumor lesions are mobile with a constantly changing position. Here, we present an innovative technique for real-time tumor tracking in cancer surgery. In this study, we evaluated the feasibility of real-time tumor tracking during rectal cancer surgery. The application of real-time tumor tracking using an intraoperative navigation system is feasible and safe with a high median target registration accuracy of 3 mm. This technique allows oncological surgeons to obtain real-time accurate information on tumor location, as well as critical anatomical information. This study demonstrates that real-time tumor tracking is feasible and could potentially decrease positive resection margins and improve patient outcome.
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http://dx.doi.org/10.1038/s41698-020-0115-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7142120PMC
April 2020

A workflow for automated segmentation of the liver surface, hepatic vasculature and biliary tree anatomy from multiphase MR images.

Magn Reson Imaging 2020 05 11;68:53-65. Epub 2020 Jan 11.

Department of Surgical Oncology, The Netherlands Cancer Institute - Antoni van Leeuwenhoek Hospital, Plesmanlaan 121, 1066 CX Amsterdam, the Netherlands; MIRA Institute of Biomedical Technology and Technical Medicine, University of Twente, Drienerlolaan 5, 7522 NB Enschede, the Netherlands.

Accurate assessment of 3D models of patient-specific anatomy of the liver, including underlying hepatic and biliary tree, is critical for preparation and safe execution of complex liver resections, especially due to high variability of biliary and hepatic artery anatomies. Dynamic MRI with hepatospecific contrast agents is currently the only type of diagnostic imaging that provides all anatomical information required for generation of such a model, yet there is no information in the literature on how the complete 3D model can be generated automatically. In this work, a new automated segmentation workflow for extraction of patient-specific 3D model of the liver, hepatovascular and biliary anatomy from a single multiphase MRI acquisition is developed and quantitatively evaluated. The workflow incorporates course 4D k-means clustering estimation and geodesic active contour refinement of the liver boundary, based on organ's characteristic uptake of gadolinium contrast agents overtime. Subsequently, hepatic vasculature and biliary ducts segmentations are performed using multiscale vesselness filters. The algorithm was evaluated using 15 test datasets of patients with liver malignancies of various histopathological types. It showed good correlation with expert manual segmentation, resulting in an average of 1.76 ± 2.44 mm Hausdorff distance for the liver boundary, and 0.58 ± 0.72 and 1.16 ± 1.98 mm between centrelines of biliary ducts and liver veins, respectively. A workflow for automatic segmentation of the liver, hepatic vasculature and biliary anatomy from a single diagnostic MRI acquisition was developed. This enables automated extraction of 3D models of patient-specific liver anatomy, and may facilitating better perception of organ's anatomy during preparation and execution of liver surgeries. Additionally, it may help to reduce the incidence of intraoperative biliary duct damage due to an unanticipated variation in the anatomy.
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http://dx.doi.org/10.1016/j.mri.2019.12.008DOI Listing
May 2020

Optimizing algorithm development for tissue classification in colorectal cancer based on diffuse reflectance spectra.

Biomed Opt Express 2019 Dec 5;10(12):6096-6113. Epub 2019 Nov 5.

Department of Surgery, Antoni van Leeuwenhoek Hospital - The Netherlands Cancer Institute, Plesmanlaan 121, 1066CX Amsterdam, The Netherlands.

Diffuse reflectance spectroscopy can be used in colorectal cancer surgery for tissue classification. The main challenge in the classification task is to separate healthy colorectal wall from tumor tissue. In this study, four normalization techniques, four feature extraction methods and five classifiers are applied to nine datasets, to obtain the optimal method to separate spectra measured on healthy colorectal wall from spectra measured on tumor tissue. All results are compared to the use of the entire non-normalized spectra. It is found that the most optimal classification approach is to apply a feature extraction method on non-normalized spectra combined with support vector machine or neural network classifier.
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http://dx.doi.org/10.1364/BOE.10.006096DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6913395PMC
December 2019

Using Diffuse Reflectance Spectroscopy to Distinguish Tumor Tissue From Fibrosis in Rectal Cancer Patients as a Guide to Surgery.

Lasers Surg Med 2020 09 3;52(7):604-611. Epub 2019 Dec 3.

Department of Surgery, Antoni van Leeuwenhoek Hospital, The Netherlands Cancer Institute, Amsterdam, 1066 CX, The Netherlands.

Background And Objectives: In patients with rectal cancer who received neoadjuvant (chemo)radiotherapy, fibrosis is induced in and around the tumor area. As tumors and fibrosis have similar visual and tactile feedback, they are hard to distinguish during surgery. To prevent positive resection margins during surgery and spare healthy tissue, it would be of great benefit to have a real-time tissue classification technology that can be used in vivo.

Study Design/materials And Methods: In this study diffuse reflectance spectroscopy (DRS) was evaluated for real-time tissue classification of tumor and fibrosis. DRS spectra of fibrosis and tumor were obtained on excised rectal specimens. After normalization using the area under the curve, a support vector machine was trained using a 10-fold cross-validation.

Results: Using spectra of pure tumor tissue and pure fibrosis tissue, we obtained a mean accuracy of 0.88. This decreased to a mean accuracy of 0.61 when tumor measurements were used in which a layer of healthy tissue, mainly fibrosis, was present between the tumor and the measurement surface.

Conclusion: It is possible to distinguish pure fibrosis from pure tumor. However, when the measurements on tumor also involve fibrotic tissue, the classification accuracy decreases. Lasers Surg. Med. © 2019 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/lsm.23196DOI Listing
September 2020

Broadband hyperspectral imaging for breast tumor detection using spectral and spatial information.

Biomed Opt Express 2019 Sep 7;10(9):4496-4515. Epub 2019 Aug 7.

Department of Surgery, Netherlands Cancer Institute, Plesmanlaan 121, 1066CX Amsterdam, Netherlands.

Complete tumor removal during breast-conserving surgery remains challenging due to the lack of optimal intraoperative margin assessment techniques. Here, we use hyperspectral imaging for tumor detection in fresh breast tissue. We evaluated different wavelength ranges and two classification algorithms; a pixel-wise classification algorithm and a convolutional neural network that combines spectral and spatial information. The highest classification performance was obtained using the full wavelength range (450-1650 nm). Adding spatial information mainly improved the differentiation of tissue classes within the malignant and healthy classes. High sensitivity and specificity were accomplished, which offers potential for hyperspectral imaging as a margin assessment technique to improve surgical outcome.
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http://dx.doi.org/10.1364/BOE.10.004496DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6757478PMC
September 2019

Toward assessment of resection margins using hyperspectral diffuse reflection imaging (400-1,700 nm) during tongue cancer surgery.

Lasers Surg Med 2020 07 15;52(6):496-502. Epub 2019 Sep 15.

Department of Surgery, Netherlands Cancer Institute, Antoni van Leeuwenhoek, Amsterdam, The Netherlands.

Background And Objectives: There is a clinical need to assess the resection margins of tongue cancer specimens, intraoperatively. In the current ex vivo study, we evaluated the feasibility of hyperspectral diffuse reflectance imaging (HSI) for distinguishing tumor from the healthy tongue tissue.

Study Design/materials And Methods: Fresh surgical specimens (n = 14) of squamous cell carcinoma of the tongue were scanned with two hyperspectral cameras that cover the visible and near-infrared spectrum (400-1,700 nm). Each pixel of the hyperspectral image represents a measure of the diffuse optical reflectance. A neural network was used for tissue-type prediction of the hyperspectral images of the visual and near-infrared data sets separately as well as both data sets combined.

Results: HSI was able to distinguish tumor from muscle with a good accuracy. The diagnostic performance of both wavelength ranges (sensitivity/specificity of visual and near-infrared were 84%/80% and 77%/77%, respectively) appears to be comparable and there is no additional benefit of combining the two wavelength ranges (sensitivity and specificity were 83%/76%).

Conclusions: HSI has a strong potential for intra-operative assessment of tumor resection margins of squamous cell carcinoma of the tongue. This may optimize surgery, as the entire resection surface can be scanned in a single run and the results can be readily available. Lasers Surg. Med. © 2019 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/lsm.23161DOI Listing
July 2020

Imaging depth variations in hyperspectral imaging: Development of a method to detect tumor up to the required tumor-free margin width.

J Biophotonics 2019 11 23;12(11):e201900086. Epub 2019 Jul 23.

Department of Surgery, Netherlands Cancer Institute, Amsterdam, the Netherlands.

Hyperspectral imaging is a promising technique for resection margin assessment during cancer surgery. Thereby, only a specific amount of the tissue below the resection surface, the clinically defined margin width, should be assessed. Since the imaging depth of hyperspectral imaging varies with wavelength and tissue composition, this can have consequences for the clinical use of hyperspectral imaging as margin assessment technique. In this study, a method was developed that allows for hyperspectral analysis of resection margins in breast cancer. This method uses the spectral slope of the diffuse reflectance spectrum at wavelength regions where the imaging depth in tumor and healthy tissue is equal. Thereby, tumor can be discriminated from healthy breast tissue while imaging up to a similar depth as the required tumor-free margin width of 2 mm. Applying this method to hyperspectral images acquired during surgery would allow for robust margin assessment of resected specimens. In this paper, we focused on breast cancer, but the same approach can be applied to develop a method for other types of cancer.
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http://dx.doi.org/10.1002/jbio.201900086DOI Listing
November 2019

Hyperspectral Imaging for Resection Margin Assessment during Cancer Surgery.

Clin Cancer Res 2019 06 18;25(12):3572-3580. Epub 2019 Mar 18.

Department of Surgery, The Netherlands Cancer Institute, Amsterdam, the Netherlands.

Purpose: Complete tumor removal during cancer surgery remains challenging due to the lack of accurate techniques for intraoperative margin assessment. This study evaluates the use of hyperspectral imaging for margin assessment by reporting its use in fresh human breast specimens.

Experimental Design: Hyperspectral data were first acquired on tissue slices from 18 patients after gross sectioning of the resected breast specimen. This dataset, which contained over 22,000 spectra, was well correlated with histopathology and was used to develop a support vector machine classification algorithm and test the classification performance. In addition, we evaluated hyperspectral imaging in clinical practice by imaging the resection surface of six lumpectomy specimens. With the developed classification algorithm, we determined if hyperspectral imaging could detect malignancies in the resection surface.

Results: The diagnostic performance of hyperspectral imaging on the tissue slices was high; invasive carcinoma, ductal carcinoma , connective tissue, and adipose tissue were correctly classified as tumor or healthy tissue with accuracies of 93%, 84%, 70%, and 99%, respectively. These accuracies increased with the size of the area, consisting of one tissue type. The entire resection surface was imaged within 10 minutes, and data analysis was performed fast, without the need of an experienced operator. On the resection surface, hyperspectral imaging detected 19 of 20 malignancies that, according to the available histopathology information, were located within 2 mm of the resection surface.

Conclusions: These findings show the potential of using hyperspectral imaging for margin assessment during breast-conserving surgery to improve surgical outcome.
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http://dx.doi.org/10.1158/1078-0432.CCR-18-2089DOI Listing
June 2019

Hyperspectral imaging for tissue classification, a way toward smart laparoscopic colorectal surgery.

J Biomed Opt 2019 01;24(1):1-9

Antoni van Leeuwenhoek Hospital, The Netherlands Cancer Institute, Department of Surgery, Amsterdam, The Netherlands.

In the last decades, laparoscopic surgery has become the gold standard in patients with colorectal cancer. To overcome the drawback of reduced tactile feedback, real-time tissue classification could be of great benefit. In this ex vivo study, hyperspectral imaging (HSI) was used to distinguish tumor tissue from healthy surrounding tissue. A sample of fat, healthy colorectal wall, and tumor tissue was collected per patient and imaged using two hyperspectral cameras, covering the wavelength range from 400 to 1700 nm. The data were randomly divided into a training (75%) and test (25%) set. After feature reduction, a quadratic classifier and support vector machine were used to distinguish the three tissue types. Tissue samples of 32 patients were imaged using both hyperspectral cameras. The accuracy to distinguish the three tissue types using both hyperspectral cameras was 0.88 (STD  =  0.13) on the test dataset. When the accuracy was determined per patient, a mean accuracy of 0.93 (STD  =  0.12) was obtained on the test dataset. This study shows the potential of using HSI in colorectal cancer surgery for fast tissue classification, which could improve clinical outcome. Future research should be focused on imaging entire colon/rectum specimen and the translation of the technique to an intraoperative setting.
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http://dx.doi.org/10.1117/1.JBO.24.1.016002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6985687PMC
January 2019

Prospective study on image-guided navigation surgery for pelvic malignancies.

J Surg Oncol 2019 Mar 24;119(4):510-517. Epub 2018 Dec 24.

Department of Surgical Oncology, Netherlands Cancer Institute-Antoni van Leeuwenhoek, Amsterdam, The Netherlands.

Background And Objectives: Surgery of advanced tumors and lymph nodes in the pelvis can be challenging due to the narrow pelvic space and vital surrounding structures. This study explores the application of a novel electromagnetic navigation system to guide pelvic surgery.

Methods: This was a prospective study on surgery for malignancies in the pelvis. Preoperatively obtained imaging was used to create a patient-specific three-dimensional (3D) roadmap. In the operating room, the 3D roadmap was registered to an intraoperative computed tomography scan. A tracked pointer was used during surgery for guidance. Primary endpoint was safety and feasibility, secondary endpoints were accuracy and usability.

Results: Twenty-eight colorectal, four liposarcomas, and one gynecological patient were included. There were no safety issues. Navigation was feasible in 31 patients. The mean target registration errors of 4.0 and 6.3 mm were achieved for straight and French position, respectively. In seven of seven patients with a locally advanced rectal tumor and in seven of eight patients with recurrences, negative margins were achieved. Thirty-three of 36 target lymph nodes were successfully removed. Surgeons using the system indicated faster localization of the tumor and improved decisiveness.

Conclusion: This novel surgical navigation system was safe and feasible during pelvic surgery and can facilitate its users.
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http://dx.doi.org/10.1002/jso.25351DOI Listing
March 2019

Towards the use of diffuse reflectance spectroscopy for real-time in vivo detection of breast cancer during surgery.

J Transl Med 2018 12 19;16(1):367. Epub 2018 Dec 19.

Department of Surgery, the Netherlands Cancer Institute-Antoni van Leeuwenhoek, Plesmanlaan 121, Postbus 90203, 1066 CX, Amsterdam, The Netherlands.

Background: Breast cancer surgeons struggle with differentiating healthy tissue from cancer at the resection margin during surgery. We report on the feasibility of using diffuse reflectance spectroscopy (DRS) for real-time in vivo tissue characterization.

Methods: Evaluating feasibility of the technology requires a setting in which measurements, imaging and pathology have the best possible correlation. For this purpose an optical biopsy needle was used that had integrated optical fibers at the tip of the needle. This approach enabled the best possible correlation between optical measurement volume and tissue histology. With this optical biopsy needle we acquired real-time DRS data of normal tissue and tumor tissue in 27 patients that underwent an ultrasound guided breast biopsy procedure. Five additional patients were measured in continuous mode in which we obtained DRS measurements along the entire biopsy needle trajectory. We developed and compared three different support vector machine based classification models to classify the DRS measurements.

Results: With DRS malignant tissue could be discriminated from healthy tissue. The classification model that was based on eight selected wavelengths had the highest accuracy and Matthews Correlation Coefficient (MCC) of 0.93 and 0.87, respectively. In three patients that were measured in continuous mode and had malignant tissue in their biopsy specimen, a clear transition was seen in the classified DRS measurements going from healthy tissue to tumor tissue. This transition was not seen in the other two continuously measured patients that had benign tissue in their biopsy specimen.

Conclusions: It was concluded that DRS is feasible for integration in a surgical tool that could assist the breast surgeon in detecting positive resection margins during breast surgery. Trail registration NIH US National Library of Medicine-clinicaltrails.gov, NCT01730365. Registered: 10/04/2012 https://clinicaltrials.gov/ct2/show/study/NCT01730365.
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http://dx.doi.org/10.1186/s12967-018-1747-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6299954PMC
December 2018

In vivo nerve identification in head and neck surgery using diffuse reflectance spectroscopy.

Laryngoscope Investig Otolaryngol 2018 Oct 9;3(5):349-355. Epub 2018 Aug 9.

Department of Surgery The Netherlands Cancer Institute-Antoni van Leeuwenhoek Amsterdam the Netherlands.

Background: Careful identification of nerves during head and neck surgery is essential to prevent nerve damage. Currently, nerves are identified based on anatomy and appearance, optionally combined with electromyography (EMG). In challenging cases, nerve damage is reported in up to 50%. Recently, optical techniques, like diffuse reflectance spectroscopy (DRS) and fluorescence spectroscopy (FS) show potential to improve nerve identification.

Methods: 212 intra-operative DRS/FS measurements were performed. Small nerve branches (1-3 mm), on near-nerve adipose tissue, muscle and subcutaneous fat were measured during 11 surgical procedures. Tissue identification was based on quantified concentrations of optical absorbers and scattering parameters.

Results: Clinically comprehensive parameters showed significant differences (<0.05) between the tissues. Classification using k-Nearest Neighbor resulted in 100% sensitivity and a specificity of 83% (accuracy 91%), for the identification of nerve against surrounding tissues.

Conclusions: DRS/FS is a potentially useful intraoperative tool for identification of nerves from adjacent tissues.

Level Of Evidence: Observational proof of principle study.
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http://dx.doi.org/10.1002/lio2.174DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6209613PMC
October 2018

Toward complete oral cavity cancer resection using a handheld diffuse reflectance spectroscopy probe.

J Biomed Opt 2018 10;23(12):1-8

Netherlands Cancer Institute, Antoni van Leeuwenhoek, Department of Surgery, Amsterdam, The Netherlands.

This ex-vivo study evaluates the feasibility of diffuse reflectance spectroscopy (DRS) for discriminating tumor from healthy tissue, with the aim to develop a technology that can assess resection margins for the presence of tumor cells during oral cavity cancer surgery. Diffuse reflectance spectra were acquired on fresh surgical specimens from 28 patients with oral cavity squamous cell carcinoma. The spectra (400 to 1600 nm) were detected after illuminating tissue with a source fiber at 0.3-, 0.7-, 1.0-, and 2.0-mm distances from a detection fiber, obtaining spectral information from different sampling depths. The spectra were correlated with histopathology. A total of 76 spectra were obtained from tumor tissue and 110 spectra from healthy muscle tissue. The first- and second-order derivatives of the spectra were calculated and a classification algorithm was developed using fivefold cross validation with a linear support vector machine. The best results were obtained by the reflectance measured with a 1-mm source-detector distance (sensitivity, specificity, and accuracy are 89%, 82%, and 86%, respectively). DRS can accurately discriminate tumor from healthy tissue in an ex-vivo setting using a 1-mm source-detector distance. Accurate validation methods are warranted for larger sampling depths to allow for guidance during oral cavity cancer excision.
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http://dx.doi.org/10.1117/1.JBO.23.12.121611DOI Listing
October 2018

Tumor Resection Margin Definitions in Breast-Conserving Surgery: Systematic Review and Meta-analysis of the Current Literature.

Clin Breast Cancer 2018 08 13;18(4):e595-e600. Epub 2018 Apr 13.

Department of Surgery, The Netherlands Cancer Institute, Amsterdam, The Netherlands; MIRA Institute, University of Twente, Enschede, The Netherlands.

Worldwide, various guidelines recommend what constitutes an adequate margin of excision for invasive breast cancer or for ductal carcinoma-in-situ (DCIS). We evaluated the use of different tumor resection margin guidelines and investigated their impact on positive margin rates (PMR) and reoperation rates (RR). Thirteen guidelines reporting on the extent of a positive margin were reviewed along with 31 studies, published between 2011 and 2016, reporting on a well-defined PMR. Studies were categorized according to the margin definition. Pooled PMR and RR were determined with random-effect models. For invasive breast cancer, most guidelines recommend a positive margin of tumor on ink. However, definitions of reported positive margins in the clinic vary from more than focally positive to the presence of tumor cells within 3 to 5 mm from the resection surface. Within the studies analyzed (59,979 patients), pooled PMRs for invasive breast cancer ranged from 9% to 36% and pooled RRs from 77% to 99%. For DCIS, guidelines vary between no DCIS on the resection surface to DCIS cells found within a distance of 2 mm from the resection edge. Pooled PMRs for DCIS varied from 4% to 23% (840 patients). Given the differences in tumor margin definition between countries worldwide, quality control data expressed as PMR or RR should be interpreted with caution. Furthermore, the overall definition for positive resection margins for both invasive disease and DCIS seems to have become more liberal.
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http://dx.doi.org/10.1016/j.clbc.2018.04.004DOI Listing
August 2018

Nerve detection during surgery: optical spectroscopy for peripheral nerve localization.

Lasers Med Sci 2018 Apr 2;33(3):619-625. Epub 2018 Feb 2.

Department of Surgery, The Netherlands Cancer Institute, Antoni van Leeuwenhoek Hospital, Plesmanlaan 121, 1066 CX, Amsterdam, The Netherlands.

Precise nerve localization is of major importance in both surgery and regional anesthesia. Optically based techniques can identify tissue through differences in optical properties, like absorption and scattering. The aim of this study was to evaluate the potential of optical spectroscopy (diffuse reflectance spectroscopy) for clinical nerve identification in vivo. Eighteen patients (8 male, 10 female, age 53 ± 13 years) undergoing inguinal lymph node resection or resection or a soft tissue tumor in the groin were included to measure the femoral or sciatic nerve and the surrounding tissues. In vivo optical measurements were performed using Diffuse Reflectance Spectroscopy (400-1600 nm) on nerve, near nerve adipose tissue, muscle, and subcutaneous fat using a needle-shaped probe. Model-based analyses were used to derive verified quantitative parameters as concentrations of optical absorbers and several parameters describing scattering. A total of 628 optical spectra were recorded. Measured spectra reveal noticeable tissue specific characteristics. Optical absorption of water, fat, and oxy- and deoxyhemoglobin was manifested in the measured spectra. The parameters water and fat content showed significant differences (P < 0.005) between nerve and all surrounding tissues. Classification using k-Nearest Neighbor based on the derived parameters revealed a sensitivity of 85% and a specificity of 79%, for identifying nerve from surrounding tissues. Diffuse Reflectance Spectroscopy identifies peripheral nerve bundles. The differences found between tissue groups are assignable to the tissue composition and structure.
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http://dx.doi.org/10.1007/s10103-017-2433-1DOI Listing
April 2018

Nerve detection using optical spectroscopy, an evaluation in four different models: In human and swine, in-vivo, and post mortem.

Lasers Surg Med 2018 03 21;50(3):253-261. Epub 2017 Nov 21.

Department of Surgery, The Netherlands Cancer Institute-Antoni van Leeuwenhoek, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands.

Objective: Identification of peripheral nerve tissue is crucial in both surgery and regional anesthesia. Recently, optical tissue identification methods are presented to facilitate nerve identification in transcutaneous procedures and surgery. Optimization and validation of such techniques require large datasets. The use of alternative models to human in vivo, like human post mortem, or swine may be suitable to test, optimize and validate new optical techniques. However, differences in tissue characteristics and thus optical properties, like oxygen saturation and tissue perfusion are to be expected. This requires a structured comparison between the models.

Study Design: Comparative observational study.

Methods: Nerve and surrounding tissues in human (in vivo and post mortem) and swine (in vivo and post mortem) were structurally compared macroscopically, histologically, and spectroscopically. Diffuse reflective spectra were acquired (400-1,600 nm) after illumination with a broad band halogen light. An analytical model was used to quantify optical parameters including concentrations of optical absorbers.

Results: Several differences were found histologically and in the optical parameters. Histologically nerve and adipose tissue (subcutaneous fat and sliding fat) showed clear similarities between human and swine while human muscle enclosed more adipocytes and endomysial collagen. Optical parameters revealed model dependent differences in concentrations of β-carotene, water, fat, and oxygen saturation. The similarity between optical parameters is, however, sufficient to yield a strong positive correlation after cross model classification.

Conclusion: This study shows and discusses similarities and differences in nerve and surrounding tissues between human in vivo and post mortem, and swine in vivo and post mortem; this could support the discussion to use an alternative model to optimize and validate optical techniques for clinical nerve identification. Lasers Surg. Med. 50:253-261, 2018. © 2017 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/lsm.22755DOI Listing
March 2018

Diffuse reflectance spectroscopy as a tool for real-time tissue assessment during colorectal cancer surgery.

J Biomed Opt 2017 Oct;22(10):1-6

Antoni van Leeuwenhoek Hospital-The Netherlands Cancer Institute, Department of Surgery, Amsterdam, The Netherlands.

Colorectal surgery is the standard treatment for patients with colorectal cancer. To overcome two of the main challenges, the circumferential resection margin and postoperative complications, real-time tissue assessment could be of great benefit during surgery. In this ex vivo study, diffuse reflectance spectroscopy (DRS) was used to differentiate tumor tissue from healthy surrounding tissues in patients with colorectal neoplasia. DRS spectra were obtained from tumor tissue, healthy colon, or rectal wall and fat tissue, for every patient. Data were randomly divided into training (80%) and test (20%) sets. After spectral band selection, the spectra were classified using a quadratic classifier and a linear support vector machine. Of the 38 included patients, 36 had colorectal cancer and 2 had an adenoma. When the classifiers were applied to the test set, colorectal cancer could be discriminated from healthy tissue with an overall accuracy of 0.95 (±0.03). This study demonstrates the possibility to separate colorectal cancer from healthy surrounding tissue by applying DRS. High classification accuracies were obtained both in homogeneous and inhomogeneous tissues. This is a fundamental step toward the development of a tool for real-time in vivo tissue assessment during colorectal surgery.
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http://dx.doi.org/10.1117/1.JBO.22.10.106014DOI Listing
October 2017

Using DRS during breast conserving surgery: identifying robust optical parameters and influence of inter-patient variation.

Biomed Opt Express 2016 Dec 17;7(12):5188-5200. Epub 2016 Nov 17.

Netherlands Cancer Institute - Antoni van Leeuwenhoek, Amsterdam The Netherlands; MIRA Institute, University Twente, The Netherlands.

Successful breast conserving surgery consists of complete removal of the tumor while sparing healthy surrounding tissue. Despite currently available imaging and margin assessment tools, recognizing tumor tissue at a resection margin during surgery is challenging. Diffuse reflectance spectroscopy (DRS), which uses light for tissue characterization, can potentially guide surgeons to prevent tumor positive margins. However, inter-patient variation and changes in tissue physiology occurring during the resection might hamper this light-based technology. Here we investigate how inter-patient variation and tissue status ( vs ) affect the performance of the DRS optical parameters. and measurements of 45 breast cancer patients were obtained and quantified with an analytical model to acquire the optical parameters. The optical parameter representing the ratio between fat and water provided the best discrimination between normal and tumor tissue, with an area under the receiver operating characteristic curve of 0.94. There was no substantial influence of other patient factors such as menopausal status on optical measurements. Contrary to expectations, normalization of the optical parameters did not improve the discriminative power. Furthermore, measurements taken were not significantly different from the measurements taken . These findings indicate that DRS is a robust technology for the detection of tumor tissue during breast conserving surgery.
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http://dx.doi.org/10.1364/BOE.7.005188DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5175562PMC
December 2016
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