Calum MacAulay

University of British Columbia - Vancouver, Vancouver, British Columbia, Canada

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Publications (339)991.66 Total impact

  • [Show abstract] [Hide abstract]
    ABSTRACT: We have built a polarization-sensitive swept source Optical Coherence Tomography (OCT) instrument capable of wide-field in vivo imaging in the oral cavity. This instrument uses a hand-held side-looking fiber-optic rotary pullback catheter that can cover two dimensional tissue imaging fields approximately 2.5 mm wide by up to 90 mm length in a single image acquisition. The catheter spins at 100 Hz with pullback speeds up to 15 mm/s allowing imaging of areas up to 225 mm(2) field-of-view in seconds. A catheter sheath and two optional catheter sheath holders have been designed to allow imaging at all locations within the oral cavity. Image quality of 2-dimensional image slices through the data can be greatly enhanced by averaging over the orthogonal dimension to reduce speckle. Initial in vivo imaging results reveal a wide-field view of features such as epithelial thickness and continuity of the basement membrane that may be useful in clinic for chair-side management of oral lesions.
    Biomedical Optics Express 07/2015; 6(7):2664-74. DOI:10.1364/BOE.6.002664 · 3.65 Impact Factor
  • European Respiratory Journal 05/2015; 46(3). DOI:10.1183/09031936.00016815 · 7.64 Impact Factor
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    ABSTRACT: DNA ploidy analysis involves automated quantification of chromosomal aneuploidy, a potential marker of progression toward cervical carcinoma. We evaluated the cost-effectiveness of this method for cervical screening, comparing five ploidy strategies (using different numbers of aneuploid cells as cut points) with liquid-based Papanicolaou smear and no screening. A state-transition Markov model simulated the natural history of HPV infection and possible progression into cervical neoplasia in a cohort of 12-year-old females. The analysis evaluated cost in 2012 US$ and effectiveness in quality-adjusted life-years (QALYs) from a health-system perspective throughout a lifetime horizon in the US setting. We calculated incremental cost-effectiveness ratios (ICERs) to determine the best strategy. The robustness of optimal choices was examined in deterministic and probabilistic sensitivity analyses. In the base-case analysis, the ploidy 4 cell strategy was cost-effective, yielding an increase of 0.032 QALY and an ICER of $18 264/QALY compared to no screening. For most scenarios in the deterministic sensitivity analysis, the ploidy 4 cell strategy was the only cost-effective strategy. Cost-effectiveness acceptability curves showed that this strategy was more likely to be cost-effective than the Papanicolaou smear. Compared to the liquid-based Papanicolaou smear, screening with a DNA ploidy strategy appeared less costly and comparably effective.British Journal of Cancer advance online publication, 28 April 2015; doi:10.1038/bjc.2015.95
    British Journal of Cancer 04/2015; 112(12). DOI:10.1038/bjc.2015.95 · 4.84 Impact Factor
  • H. Pahlevaninezhad · A.M.D. Lee · R. Marsh · S. Lam · C. MacAulay · P. Lane
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    ABSTRACT: This work reports a fiber optic-based endoscopic imaging system capable of combined Doppler optical coherence tomography (DOCT) and autofluorescence (AF) imaging. The two key components in this dual-modality imaging system are a specially designed three-port wavelength multiplexing fiber optic rotary joint (FORJ) and a custom 900 μm diameter double-clad fiber (DCF) catheter. The three-port FORJ combines the two imaging modalities efficiently with more than 83% throughput for collected AF emission and the DCF catheter allows endoscopic coregistered DOCT and AF imaging. Endoscopic DOCT and AF imaging of small human airways in vivo is presented to demonstrate the performance of the system.
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    ABSTRACT: Although the Papanicolaou smear has been successful in decreasing cervical cancer incidence in the developed world, there exist many challenges for implementation in the developing world. Quantitative cytology, a semi-automated method that quantifies cellular image features, is a promising screening test candidate. The nested structure of its data (measurements of multiple cells within a patient) provides challenges to the usual classification problem. Here we perform a comparative study of three main approaches for problems with this general data structure: (i) extract patient-level features from the cell-level data, (ii) use a statistical model that accounts for the hierarchical data structure, and (iii) classify at the cellular level and use an ad hoc approach to classify at the patient level. We apply these methods to a dataset of 1728 patients, with an average of 2600 cells collected per patient and 133 features measured per cell, predicting whether a patient had a positive biopsy result. The best approach we found was to classify at the cellular level and count the number of cells that had a posterior probability greater than a threshold value, with estimated 61% sensitivity and 89% specificity on independent data. Recent statistical learning developments allowed us to achieve high accuracy.
    Statistical Analysis and Data Mining 04/2015; 8(2). DOI:10.1002/sam.11261
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    ABSTRACT: Volatile Organic Compounds (VOC) in exhaled breath as measured by electronic nose (e-nose) have utility as biomarkers to detect subjects at ris of having lung cancer in a screening setting. We hypothesize that breath analysis using an e-nose chemo-resistive sensor array could be used as a screening tool to discriminate patients diagnosed with lung cancer from high-risk smokers. Breath samples from 191 subjects - 25 lung cancer patients and 166 high-risk smoker control subjects without cancer - were analyzed. For clinical relevancy, subjects in both groups were matched for age, sex, and smoking histories. Classification and Regression Trees and Discriminant Functions classifiers were used to recognize VOC patterns in e-nose data. Cross-validated results were used to assess classification accuracy. Repeatability and reproducibility of e-nose data were assessed by measuring subject-exhaled breath in parallel across two e-nose devices. E-nose measurements could distinguish lung cancer patients from high-risk control subjects, with a better than 80% classification accuracy. Subject sex and smoking status impacted classification as area under the curve results (ex-smoker males 0.846, ex-smoker female 0.816, current smoker male 0.745 and current smoker female 0.725) demonstrated. Two e-nose systems could be calibrated to give equivalent readings across subject-exhaled breath measured in parallel. E-nose technology may have significant utility as a non-invasive screening tool for detecting individuals at increased risk for lung cancer. The results presented further the case that VOC patterns could have real clinical utility to screen for lung cancer in the important growing ex-smoker population.
    IEEE transactions on bio-medical engineering 03/2015; 62(8). DOI:10.1109/TBME.2015.2409092 · 2.35 Impact Factor
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    ABSTRACT: Diagnosis of peripheral lung nodules is challenging because they are rarely visualized endobronchially. Imaging techniques such as endobronchial ultrasound (EBUS) are employed to improve tumor localization. The current EBUS probe provides limited nodule characterization and has an outer diameter of 1.4 mm that restricts access to small peripheral airways. We report a novel co-registered autofluoresence Doppler optical coherence tomography (AF/DOCT) system with a 0.9 mm diameter probe to characterize peripheral lung nodules prior to biopsy in vivo. Method: Patients referred for evaluation of peripheral lung nodules underwent bronchoscopy with examination of standard EBUS and the novel AF/DOCT system. The lesion of interest was first identified with EBUS and then imaged with the AF/DOCT system. The abnormal area was biopsied. AF/DOCT images of pathology proved lung malignancies were reviewed by a panel of a pathologist, respirologists, and AF/DOCT experts. Results: Eleven patients with biopsy proven lung cancer underwent examination with AF/DOCT. The majority of the cancers were adenocarcinoma. AF/DOCT images were obtained in all patients. There were no complications to the procedures. Lung abnormalities visualized in AF/OCT images were observed in 11 cases. In one case large blood vessels were identified and biopsy was avoided. Conclusion: In this pilot study, AF/DOCT obtained high quality images of peripheral pulmonary nodules. The present study supports the safety and feasibility of AF/DOCT for the evaluation of lung cancer. The addition of Doppler information may improve biopsy site selection and reduce hemorrhage.
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    ABSTRACT: We examined and established the potential of ex-vivo confocal fluorescence microscopy for differentiating between normal cervical tissue, low grade Cervical Intraepithelial Neoplasia (CIN1), and high grade CIN (CIN2 and CIN3). Our objectives were to i) use Quantitative Tissue Phenotype (QTP) analysis to quantify nuclear and cellular morphology and tissue architecture in confocal microscopic images of fresh cervical biopsies and ii) determine the accuracy of high grade CIN detection via confocal microscopy. Cervical biopsy specimens of colposcopically normal and abnormal tissues obtained from 15 patients were evaluated by confocal fluorescence microscopy. Confocal images were analyzed and about 200 morphological and architectural features were calculated at the nuclear, cellular, and tissue level. For the purpose of this study, we used four features to delineate disease grade including nuclear size, cell density, estimated nuclear-cytoplasmic (ENC) ratio, and the average of three nearest Delaunay neighbors distance (3NDND). Our preliminary results showed ENC ratio and 3NDND correlated well with histopathological diagnosis. The Spearman correlation coefficient between each of these two features and the histopathological diagnosis was higher than the correlation coefficient between colposcopic appearance and histopathological diagnosis. Sensitivity and specificity of ENC ratio for detecting high grade CIN were both equal to 100%. QTP analysis of fluorescence confocal images shows the potential to discriminate high grade CIN from low grade CIN and normal tissues. This approach could be used to help clinicians identify HGSILs in clinical settings.
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    ABSTRACT: For the first time, we present co-registered autofluorescence imaging and optical coherence tomography (AF/OCT) of excised human palatine tonsils to evaluate the capabilities of OCT to visualize tonsil tissue components. Despite limited penetration depth, OCT can provide detailed structural information about tonsil tissue with much higher resolution than that of computed tomography, magnetic resonance imaging, and Ultrasound. Different tonsil tissue components such as epithelium, dense connective tissue, lymphoid nodules, and crypts can be visualized by OCT. The co-registered AF imaging can provide matching biochemical information. AF/OCT scans may provide a non-invasive tool for detecting tonsillar cancers and for studying the natural history of their development.
    PLoS ONE 12/2014; 9(12):e115889. DOI:10.1371/journal.pone.0115889 · 3.23 Impact Factor
  • C. Poh · S. Durham · P. Brasher · K. Berean · C. MacAulay · M. Rosin
    Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology 11/2014; 118(6). DOI:10.1016/j.oooo.2014.05.060 · 1.46 Impact Factor
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    ABSTRACT: Cigarette smoke is associated with the majority of lung cancers: however, 25% of lung cancer patients are non-smokers, and half of all newly diagnosed lung cancer patients are former smokers. Lung tumors exhibit distinct epidemiological, clinical, pathological, and molecular features depending on smoking status, suggesting divergent mechanisms underlie tumorigenesis in smokers and non-smokers. MicroRNAs (miRNAs) are integral contributors to tumorigenesis and mediate biological responses to smoking. Based on the hypothesis that smoking-specific miRNA differences in lung adenocarcinomas reflect distinct tumorigenic processes selected by different smoking and non-smoking environments, we investigated the contribution of miRNA disruption to lung tumor biology and patient outcome in the context of smoking status. We applied a whole transcriptome sequencing based approach to interrogate miRNA levels in 94 patient-matched lung adenocarcinoma and non-malignant lung parenchymal tissue pairs from current, former and never smokers. We discovered novel and distinct smoking status-specific patterns of miRNA and miRNA-mediated gene networks, and identified miRNAs that were prognostically significant in a smoking dependent manner. We conclude that miRNAs disrupted in a smoking status-dependent manner affect distinct cellular pathways and differentially influence lung cancer patient prognosis in current, former and never smokers. Our findings may represent promising biologically relevant markers for lung cancer prognosis or therapeutic intervention.
    BMC Cancer 10/2014; 14(1):778. DOI:10.1186/1471-2407-14-778 · 3.36 Impact Factor
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    ABSTRACT: Purpose: DNA ploidy analysis, a semi-automated process, has been proposed as a potential alternative for cervical screening; however, this strategy has not been evaluated economically. Our study examined the cost-effectiveness of ploidy analysis in comparison to liquid-based Papanicolaou (Pap) smear in the screening setting. Methods: The use of ploidy was examined with five thresholds corresponding to the number (from 1 to 5) of aneuploid cells in a specimen. For example, the ploidy 3 cell strategy rendered a specimen abnormal if at least 3 aneuploid cells were found. We compared these five ploidy strategies and the liquid-based Pap smear with a no screening strategy as the reference. We developed a state-transition Markov model to simulate the natural history of HPV infection and possible progression into cervical neoplasia in a hypothetical cohort of 12-year-old females (started triennial screening from 21 years). The analysis was conducted using cost in 2012 US$ and effectiveness in quality-adjusted life-years (QALYs) from a health-system perspective throughout a lifetime horizon in the US setting. The willingness-to-pay threshold was $50,000/QALY. We calculated the incremental cost-effectiveness ratios (ICERs) for the various strategies to determine the best ploidy strategy and the overall recommended strategy. The robustness of optimal choices was examined in deterministic and probabilistic sensitivity analyses. Results: In the base-case analysis, the ploidy 4 cell strategy was cost-effective. It increased the quality-adjusted life expectancy by 0.083 QALY and yielded an ICER of $8,774/QALY compared to the no screening strategy. In the deterministic sensitivity analysis, the cost-effectiveness was most sensitive to the cost of the Pap smear procedure, the cost of treating high-grade squamous intraepithelial lesions, the cost of the ploidy analysis, and the ploidy strategies' operating characteristics. For most scenarios, the ploidy 4 cell strategy was cost-effective and was considered the best ploidy strategy. The cost-effectiveness acceptability curves showed that the ploidy 4 cell strategy was more likely to be cost-effective than the Pap smear strategy. Conclusion: Compared to liquid-based Pap smear screening, ploidy analysis appeared less costly and comparably effective using the standard willingness-to-pay threshold. Screening for cervical neoplasia using DNA ploidy analysis may be a satisfactory alternative, particularly in low-infrastructure settings. Figure 1. Cost-effectiveness acceptability curves comparing no screening, Papanicolaou smear screening, and the ploidy 4 cell strategy.
    The 36th Annual Meeting of the Society for Medical Decision Making; 10/2014
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    ABSTRACT: Worldwide, oral cancer is responsible for 170,000 deaths per year. Intervention to prevent this disease is a long sought after goal. Chemoprevention studies have focused on clinicopathological features of potentially malignant lesions (PML) in an effort to prevent their progression to cancer. However, prediction of future behavior for such lesions is difficult and remains a major challenge to such intervention. Different approaches to this problem have been tested in the past 20years. Early genetic progression models identified critical regions of allelic imbalance at 3p and 9p, and provided the basis for molecular markers to identify progressing PMLs. Subsequently, technological advances, such as genome-wide high-throughput array platforms, computer imaging, visualization technology and next generation sequencing, have broadened the scope for marker development and have the potential of further improving our ability to identify high-risk lesions in the near future either alone or in combination. In this article, we examine the milestones in the development of markers for PML progression. We emphasize the critical importance of networks among scientists, health professionals and community to facilitate the validation and application of putative markers into clinical practice. With a growing number of new agents to validate, it is necessary to coordinate the design and implementation of strategies for patient recruitment, integration of marker assessment, and the final translation of such approaches into clinical use.
    Oral Oncology 09/2014; 50(12). DOI:10.1016/j.oraloncology.2014.08.012 · 3.61 Impact Factor
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    ABSTRACT: Accurate cervical intra-epithelial neoplasia (CIN) lesion grading is needed for effective patient management. We applied computer-assisted scanning and analytic approaches to immuno-stained CIN lesion sections to more accurately delineate disease states and decipher cell proliferation impacts from HPV and smoking within individual epithelial layers. A patient cohort undergoing cervical screening was identified (n = 196) and biopsies of varying disease grades and with intact basement membranes and epithelial layers were obtained (n = 261). Specimens were sectioned, stained (Mib1), and scanned using a high-resolution imaging system. We achieved semi-automated delineation of proliferation status and epithelial cell layers using Otsu segmentation, manual image review, Voronoi tessellation, and immuno-staining. Data were interrogated against known status for HPV infection, smoking, and disease grade. We observed increased cell proliferation and decreased epithelial thickness with increased disease grade (when analyzing the epithelium at full thickness). Analysis within individual cell layers showed a ≥50% increase in cell proliferation for CIN2 vs. CIN1 lesions in higher epithelial layers (with minimal differences seen in basal/parabasal layers). Higher rates of proliferation for HPV-positive vs. -negative cases were seen in epithelial layers beyond the basal/parabasal layers in normal and CIN1 tissues. Comparing smokers vs. non-smokers, we observed increased cell proliferation in parabasal (low and high grade lesions) and basal layers (high grade only). In sum, we report CIN grade-specific differences in cell proliferation within individual epithelial layers. We also show HPV and smoking impacts on cell layer-specific proliferation. Our findings yield insight into CIN progression biology and demonstrate that rigorous, semi-automated imaging of histopathological specimens may be applied to improve disease grading accuracy.
    PLoS ONE 09/2014; 9(9):e107088. DOI:10.1371/journal.pone.0107088 · 3.23 Impact Factor
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    ABSTRACT: We present a power-efficient fiber-based imaging system capable of co-registered autofluorescence imaging and optical coherence tomography (AF/OCT). The system employs a custom fiber optic rotary joint (FORJ) with an embedded dichroic mirror to efficiently combine the OCT and AF pathways. This three-port wavelength multiplexing FORJ setup has a throughput of more than 83% for collected AF emission, significantly more efficient compared to previously reported fiber-based methods. A custom 900 µm diameter catheter ‒ consisting of a rotating lens assembly, double-clad fiber (DCF), and torque cable in a stationary plastic tube ‒ was fabricated to allow AF/OCT imaging of small airways in vivo. We demonstrate the performance of this system ex vivo in resected porcine airway specimens and in vivo in human on fingers, in the oral cavity, and in peripheral airways.
    Biomedical Optics Express 09/2014; 5(9). DOI:10.1364/BOE.5.002978 · 3.65 Impact Factor
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    Sara A MacLellan · Calum MacAulay · Stephen Lam · Cathie Garnis
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    ABSTRACT: Background MicroRNAs (miRNAs) are non-coding RNAs that negatively regulate gene expression by preventing the translation of specific mRNA transcripts. Recent studies have shown that miRNAs are stably expressed in human serum samples, making them good candidates for the non-invasive detection of disease. However, before circulating miRNAs can be used reliably as biomarkers of disease, the pre-measurement variables that may affect serum miRNA levels must be assessed. Methods In this study we used quantitative RT-PCR to examine the effect of hemolysis, fasting, and smoking on the levels of 742 miRNAs in the serum of healthy individuals. We also compared serum miRNA profiles of samples taken from healthy individuals over different time periods to assess normal serum miRNA fluctuations. Results We have found that mechanical hemolysis of blood samples can significantly alter serum miRNA quantification and have identified 162 miRNAs that are significantly up-regulated in hemolysed serum samples. Conversely, fasting and smoking were demonstrated to not have a significant effect on the overall serum miRNA profiles of healthy individuals. The serum miRNA profiles of matched samples taken from individuals over varying time periods showed a high correlation and no miRNAs were significantly differentially expressed in these samples further suggesting the utility of serum miRNAs as biomarkers of disease. Taking the above results into consideration, we have identified miR-99a-5p and miR-139-5p as novel endogenous controls for serum miRNA studies due to their consistency across all sample sets. Conclusion These results identify important pre-profiling factors that should be taken into consideration when identifying endogenous controls and candidate biomarkers for circulating miRNA studies.
    BMC Clinical Pathology 06/2014; 14(1):27. DOI:10.1186/1472-6890-14-27
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    ABSTRACT: Examining and quantifying changes in airway morphology is critical for studying longitudinal pathogenesis and interventions in diseases such as chronic obstructive pulmonary disease and asthma. Here we present fiber-optic optical coherence tomography (OCT) as a nondestructive technique to precisely and accurately measure the 2-dimensional cross-sectional areas of airway wall substructure divided into the mucosa (WAmuc), submucosa (WAsub), cartilage (WAcart), and the airway total wall area (WAt). Porcine lung airway specimens were dissected from freshly resected lung lobes (N = 10). Three-dimensional OCT imaging using a fiber-optic rotary-pullback probe was performed immediately on airways greater than 0.9 mm in diameter on the fresh airway specimens and subsequently on the same specimens post-formalin-fixation. The fixed specimens were serially sectioned and stained with H&E. OCT images carefully matched to selected sections stained with Movat's pentachrome demonstrated that OCT effectively identifies airway epithelium, lamina propria, and cartilage. Selected H&E sections were digitally scanned and airway total wall areas were measured. Traced measurements of WAmuc, WAsub, WAcart, and WAt from OCT images of fresh specimens by two independent observers found there were no significant differences (p>0.05) between the observer's measurements. The same wall area measurements from OCT images of formalin-fixed specimens found no significant differences for WAsub, WAcart and WAt, and a small but significant difference for WAmuc. Bland-Altman analysis indicated there were negligible biases between the observers for OCT wall area measurements in both fresh and formalin-fixed specimens. Bland-Altman analysis also indicated there was negligible bias between histology and OCT wall area measurements for both fresh and formalin-fixed specimens. We believe this study sets the groundwork for quantitatively monitoring pathogenesis and interventions in the airways using OCT.
    PLoS ONE 06/2014; 9(6):e100145. DOI:10.1371/journal.pone.0100145 · 3.23 Impact Factor
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    ABSTRACT: We report a polarization diversity detection scheme for optical coherence tomography with a new, custom, miniaturized fiber coupler with single mode (SM) fiber inputs and polarization maintaining (PM) fiber outputs. The SM fiber inputs obviate matching the optical lengths of the X and Y OCT polarization channels prior to interference and the PM fiber outputs ensure defined X and Y axes after interference. Advantages for this scheme include easier alignment, lower cost, and easier miniaturization compared to designs with free-space bulk optical components. We demonstrate the utility of the detection system to mitigate the effects of rapidly changing polarization states when imaging with rotating fiber optic probes in Intralipid suspension and during in vivo imaging of human airways.
    Optics Letters 06/2014; 39(12):3638-3641. DOI:10.1364/OL.39.003638 · 3.29 Impact Factor
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    ABSTRACT: A major challenge for the early diagnosis of oral cancer is the ability to differentiate oral premalignant lesions (OPL) at high risk of progressing into invasive squamous cell carcinoma (SCC) from those at low risk. Our group has previously used high-resolution image analysis algorithms to quantify the nuclear phenotypic changes occurring in OPLs. This approach, however, requires a manual selection of nuclei images. Here, we investigated a new, semi-automated algorithm to identify OPLs at high risk of progressing into invasive SCC from those at low risk using Random Forests, a tree-based ensemble classifier. We trained a sequence of classifiers using morphometric data calculated on nuclei from 29 normal, 5 carcinoma in situ (CIS) and 28 SCC specimens. After automated discrimination of nuclei from other objects (i.e., debris, clusters, etc.), a nuclei classifier was trained to discriminate abnormal nuclei (8,841) from normal nuclei (5,762). We extracted voting scores from this trained classifier and created an automated nuclear phenotypic score (aNPS) to identify OPLs at high risk of progression. The new algorithm showed a correct classification rate of 80 % (80.6 % sensitivity, 79.3 % specificity) at the cellular level for the test set, and a correct classification rate of 75 % (77.8 % sensitivity, 71.4 % specificity) at the tissue level with a negative predictive value of 76 % and a positive predictive value of 74 % for predicting progression among 71 OPLs, performed on par with the manual method in our previous study. We conclude that the newly developed aNPS algorithm serves as a crucial asset in the implementation of high-resolution image analysis in routine clinical pathology practice to identify lesions that require molecular evaluation or more frequent follow-up.
    05/2014; 37(3). DOI:10.1007/s13402-014-0172-x
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    ABSTRACT: We are investigating spectroscopic devices designed to make in vivo cervical tissue measurements to detect pre-cancerous and cancerous lesions. All devices have the same design and ideally should record identical measurements. However, we observed consistent differences among them. An experiment was designed to study the sources of variation in the measurements recorded. Here we present a log additive statistical model that incorporates the sources of variability we identified. Based on this model, we estimated correction factors from the experimental data needed to eliminate the inter-device variability and other sources of variation. These correction factors are intended to improve the accuracy and repeatability of such devices when making future measurements on patient tissue.
    Optics Express 04/2014; 22(7):7617-24. DOI:10.1364/OE.22.007617 · 3.49 Impact Factor

Publication Stats

7k Citations
991.66 Total Impact Points


  • 1988–2015
    • University of British Columbia - Vancouver
      • • Department of Obstetrics and Gynaecology
      • • Cell and Developmental Biology (CELL)
      • • Department of Pathology and Laboratory Medicine
      • • Department of Dermatology and Skin Science
      • • Faculty of Medicine
      Vancouver, British Columbia, Canada
  • 1988–2014
    • BC Cancer Research Centre
      • Integrative Oncology Department
      Vancouver, British Columbia, Canada
  • 1999–2013
    • BC Cancer Agency
      Vancouver, British Columbia, Canada
  • 2002–2008
    • Rice University
      • Department of Chemistry
      Houston, TX, United States
  • 2007
    • University of Santiago, Chile
      CiudadSantiago, Santiago Metropolitan, Chile
    • Vancouver Coastal Health
      Vancouver, British Columbia, Canada
    • University of Houston
      Houston, Texas, United States
    • Johns Hopkins University
      Baltimore, Maryland, United States
  • 2006
    • University of Texas at Austin
      • Department of Biomedical Engineering
      Austin, Texas, United States
  • 2005
    • The International Society for Optics and Photonics
      International Falls, Minnesota, United States
  • 2004–2005
    • University of Texas at Dallas
      Richardson, Texas, United States
    • Michael Smith Genome Sciences Centre
      Calgary, Alberta, Canada
  • 2003–2004
    • University of Texas MD Anderson Cancer Center
      Houston, Texas, United States
  • 2001
    • Justus-Liebig-Universität Gießen
      • Institute of Parasitology
      Giessen, Hesse, Germany
  • 1994
    • University of Guelph
      • College of Biological Science
      Guelph, Ontario, Canada
  • 1992
    • The University of Manchester
      Manchester, England, United Kingdom