Measurements with small animal MRI were done on the 4th, 8th, 11th, 15th, 18th and 23rd days of the experiment in Phase III/3. The shape of the tumor, more often than not, is not an ellipsoid. CAS J. Nucl. Figure 19. Bevacizumab (Avastin) [1] is an exogenous inhibitor, which inhibits the biological activity of human VEGF [2]. After staining, fluorescence pictures were done from the slides using confocal microscope (BIO-RAD MRC-1024). Finally, it finds the volume between these two surfaces and sets this to be the volume of the tumor (shaded red region in Figure 11, red region in Figure 14 below). It means that a mouse of the case group received 1.11 g bevacizumab (with 45 l 0.9% NaCl solution) every day from the 3rd day for 20 days. We compared tumor volumes estimated in vivo by BLI and FLI, to those calculated by caliper measurements and found a good correlation between these two techniques (Figure 4). Ergonomics 37, 217229 (1994). N-nitrosomethylurea as mammary gland carcinogen in rats. Accuracy of Optical Imaging for Measuring Tumor Burden In Vivo . Folia Biol. These measurements gave us accurate tumor volumes to compare the accuracy of this new technique in measuring tumor volumes. In caliper measurements, two values, for length and width, must be recorded for one tumor in each animal; this means that for every 100 animals studied, at least 200 measurements must be made and recorded. . Similarly, we may have the possibility to a) measure the tumor volume using nanotechnology, b) create a pump for drug administration and c) design control algorithms for specific tumor types. Finding the mathematical relationship between MRI-measured tumor volume and tumor mass creates the possibility to estimate tumor volume from caliper-measured data. Notice that the red dots are generally underestimations, while the blue squares are generally overestimations; the former is because of the unmeasured part of the tumor, as discussed in Section 3.5, and the fact that tumors tend to grow under the surface of the skin rather than above it in their early stages of development, and the latter is because of the inherent overestimation in the industry-standard caliper-based formula. In this study, the authors measured dimensions of rat mammary tumors using a caliper and using real-time compound B-mode ultrasonography. We found out that due to this unmeasured part, the dissected tumor volumes were about 6% larger than the scan results. The other eight tumors exhibit forms that cannot be compared to a perfect ellipsoid. Epub 2013 Jul 11. Read the article on why you should not use calipers! 39, 16 (1996). Repetitive non-typhoidal Salmonella exposure is an environmental risk factor for colon cancer and tumor growth. For more information about PLOS Subject Areas, click Res. Tumor was located in the last third of the back in every cases, thus the effect of respiratory movement was minimal. Investigating the results of Phase III/3 one can observe that the two-dimensional mathematical model has good estimation property when the tumor width and length values are small; however, for large tumor diameter values the estimation could result in significant error, the estimated value is greater than the measured one (outliers are E8, C2). Figure 6. depicts three components used to measure the volume of a tumor: its length, represented by blue arrows, its width by green, and its height by yellow. The caliper, unlike the scanner, does not consider that the height of the stack changes while the length and width remain the same. Analysis of Variance (ANOVA) test was used to compare more than two samples, while pairwise comparison was done by Tukeys honest significant difference (HSD) test. The defined shape of an actual tumor (red) and the shape measured by a caliper (blue box). Evaluation of prostate volume by transabdominal ultrasonography with modified ellipsoid formula at different stages of benign prostatic hyperplasia. Tumor volumes ranged from 0.5 cc to 187.9 cc, with a median of 21.8 cc. The article discusses two results. It can be carried out in vivo during the experiment due to the subcutaneous localization of the tumor. Bizberg Themes, By Memorial Sloan Kettering Cancer Center. The .gov means its official. https://doi.org/10.1371/journal.pone.0142190.t003. Get the most important science stories of the day, free in your inbox. Med. 20, the red dots that represent scanner-based measurements are closer to the black dotted (objective) line than the blue squares that represent caliper-based measurements. The tumor dimensions are L, W, and H. The volume of an ellipsoid VE, using the variables as shown in Figure 1., is. Experimentally induced mammary tumors in rats. At this critical stage in the tumors growth, the caliper-based volume measurement will generally be larger than the tumors actual volume, since the longest axis of the parallelepiped will be partially empty. Figure 7. However mice which were treated with a quasi-continuous therapy (one-tenth dose of control dose spread over 18 days, i.e. Copyright 2023 This process not only deforms the tumor mass but also creates undesirable pain on the animal. Because the industrys caliper-based formula allows for these inclusions in nonexistent volumes more often than not, it yields inaccurate measurements, which can confuse. Cancer Res. Designed by If one measures the volume of a penny using calipers and uses the widely accepted formula, repeating the measurement each time another penny is added to the stack, the stack will yield the same volume each time, regardless of how many pennies are stacked. Because tumor volume measurements used by researchers and industries are sensitive and often rely on the accuracy, the cutting-edge TumorImagerTM line of scanners is the ideal, most reliable choice for taking such sensitive measurements. produced by the TumorImager-2TM so that the animal is aligned under the mask each time similarly to the previous scan. The explanation of the effectiveness of low dose VEGF therapy is the following ([3944]). (6) (7). One can see experimental settings in Table 1, while MRI image of a control group mouse (C4) that was measured at the end of the experiment can be found in Fig 3. https://doi.org/10.1371/journal.pone.0142190.t001, https://doi.org/10.1371/journal.pone.0142190.g003. No, Is the Subject Area "Breast cancer" applicable to this article? The effectiveness of bevacizumab administration was examined by statistical analysis. . PhD from the 1st Department of Pathology and Experimental Cancer Research Institute from Semmelweis University, Budapest, for making the fluorescence pictures with confocal microscope. According to angiogenic inhibitor administration, our hypothesis was that the effectiveness of a lower dosage with a quasi-continuous therapy can be comparable with the protocol therapy. We have examined C38 mouse colon adenocarcinoma and HT-29 human colorectal adenocarcinoma. Then we calculated the Coefficient of Variance between such measurements for both measurements to compare average inter-operator differences. & Deshayes, J.L. A 3-D illustration can be found in Fig 7. a) berry-shaped tumor; b) x-diameter of the tumor; c) y-diameter of the tumor; d) z-diameter of the tumor; e) berry-shaped tumor with ellipsoidal estimation. A smaller diameter mask will help to position the tumor in the center of the scan, but it will not alter this effect. Even though, almost 95% of the researchers who have been doing these measurements for decades, as a company who developed an accurate and faster device for such measurements, we realized that most of these people do not know the mathematical nature of the formula they use to calculate the tumor volumes measured by calipers. Treat. The mathematical relationship between MRI-measured tumor volume and mass was investigated to estimate accurate tumor volume using caliper-measured data. Denis, F., Paon, L. & Tranquart, F. Radiosensitivity of rat mammary tumors correlates with early vessel changes assessed by Power Doppler sonography. (3), Another relatively new but not widely used approach to estimate tumor volume is to assume hemi-ellipsoid shape [24]. The TM900 also stores an optical image in the measurement data base. Also, at beginning of the tumor growth when the tumor is invisible or when a tumor shrinks due to the effectiveness of the drug, in order to measure the volume of such an invisible tumor, it is a general practice to palpate the tumor area to reveal some mass to measure. Tumor size was measured every 3 days using a digital caliper and computed according to the ellipsoidal calculation formula: V . 1 0 obj However, if the treatment is lengthy, the problem of side-effects also has to be considered. (Inbred C57Bl/6 mice from our institute were used throughout the studies.) When the tumors became palpable, measurements of tumor volume were performed (with calipers) once per week. Watch our 2-minute video overview. Accurately measure the tumor (in cm) using a caliper. Figure 5. Breathing was monitored with piezoelectric transducer; temperature of the body was measured by rectal thermometer. where f is a constant which belongs to a certain tumor type. Since 2004, the target therapy of bevacizumab (Avastin) is widely used to treat colorectal [9], kidney [10], cervical [34], ovarian [35], non-small cell lung cancers [5], melanoma [14] and certain brain tumors (e.g. Using an extremely low dosage (as in our study), there is a high probability that these adverse effects can be minimized. A caliper only digitizes the length and width of the tumor. A direct 3d measurement tool such as the TM900 does not induce such method sensitivity but cannot exclude operator dependency of the obtained values. These model-based protocols can be more effective than the current ones, since they provide individual treatment for the patients. (2), Whilst studies have shown that tumors can be better estimated with ellipsoid shape than using Eq 1, calculating the volume of an ellipsoid requires the knowledge of the third parameter. where V m is the measurement threshold that represents the smallest measurable tumor volume using a caliper. Additionally, we explore the impact of six different tumour . The height and topography of the tumor is not taken into account in a caliper measurement. Pathol. Tumor volume was measured in two different ways. For this dataset, linear curve fitting was carried out (fitted linear curve) to find the mathematical relationship between MRI-measured tumor volume and tumor mass. During the scan, a mouse should be held in a relaxed manner without stretching its skin to cause unwanted deformation of the tumor body. and transmitted securely. In Phase IV, eleven weeks old male SCID mice with implanted HT-29 human colorectal adenocarcinoma was used. Google Scholar. This results in the inclusion of sections of the parallelepipeds volume that does not exist in the actual tumor. This concept can easily be understood by a simple thought experiment: the volume of a stack of pennies (Figure 4.). Ultrasonographic, thermographic and histologic evaluation of MNU-induced mammary tumors in female Sprague-Dawley rats. Based on the experimental data, model identification can be carried out which describes the mathematical model of the investigated biological process. . These images also provide extra morphological information about the tumor growth and the effect of the compounds on tumor behavior. Figure 16. depicts the results from a study attended by Biopticon in which ten subcutaneous tumors in mice were measured by scanner and caliper by four operators. Russo J, Russo IH, Rogers AE, van Zwieten MJ, Gusterson B. Toxicol Pathol. Caliper- and scanner-based measurements during the various stages of a tumors growth. Is the Subject Area "Cancers and neoplasms" applicable to this article? Tumours of the mammary gland. The problems with tumor volume measurements by calipers 3.1 Tumor growth: Height is not equal to the width of the tumor . Most, if not all, tumors do not fit into this category; this discrepancy results in caliper-based volume measurements including sections that do not exist in the actual tumor, or an overestimation of tumor volume measurement. The second result which is discussed in the article is comparison of the effectiveness of bevacizumab administration in the case of protocol-based and quasi-continuous therapies. Measurement by Caliper In order to estimate tumor volume by external caliper, the greatest longitudinal diameter (length) and the FOIA ), the more correlated a given group (scanner or caliper estimations) is to the black line (r2 = 1), the more accurate the tumor volume measurements are. & Lin, C.A. 19, 6170 (1989). Notice that in the caliper group, the average standard deviation is larger than that of the group whose tumors were measured by Biopticons TumorImager scanner. Russo, J. Comp. Oncol. Quantity of the optimal solvent administration was also examined in this subphase. Inhibiting the glycerophosphodiesterase EDI3 in ER-HER2+ breast cancer cells resistant to HER2-targeted therapy reduces viability and tumour growth. We have found that mice which have received therapy had tumor with irregular, and in several cases berry-shaped structure, especially when reaching large volume. () and were used with the parameters displayed in Table 1Parameters for Gompertz growth were taken from Benzekry et al. Pritt, B., Ashikaga, T., Oppenheimer, R.G. For small tumors, the error is about 7%, while for large tumors it is 27%.[3]. Komrek, V. Gross anatomy. Department of Veterinary Sciences, University of Trs-os-Montes and Alto Douro, Vila Real, Portugal, Ana Faustino-Rocha, Jacinta Pinho-Oliveira, Catarina Teixeira-Guedes& Ruben Soares-Maia, Department of Veterinary Sciences, Animal and Veterinary Research Centre, University of Trs-os-Montes and Alto Douro, Vila Real, Portugal, Paula A. Oliveira, Bruno Colao, Maria Joo Pires& Jorge Colao, Laboratory for Process, Environmental and Energy Engineering, Faculty of Engineering, University of Porto, Porto, Portugal, Faculty of Veterinary Medicine of Lusophone University of Humanities and Technologies, Lisboa, Portugal, Department of Chemistry, Organic Chemistry of Natural Products and Agrifood, Mass Spectrometry Center, University of Aveiro, Aveiro, Portugal, Department of Veterinary Sciences, Centre for Research and Technology of Agro-Environment and Biological Sciences, University of Trs-os-Montes and Alto Douro, Vila Real, Portugal, You can also search for this author in The value w (width) is the smaller of two perpendicular tumor axes and the value l . Tumor growth Tumor regression Number of Number of volume volume doublings Percentage additional halvings: Decrease in Percentage decrcase in increase Volume Area" Diameterb volume doubling number Volume Area" Diameterb Doubling of Halving of Volume 1 .o 100.0 58.7 26.0 Volume 1 .o 50.0 37.0 20.6 Mice were monitored daily by personnel experienced in recognizing signs of morbidity (illness, injury, or abnormal behavior) also in weekends and holidays. Mammary tumors seemed to take on an oblate spheroid geometry. Figure 16. The second subphase (Phase III/2) was similar to Phase III/1, mice received the same dosage of bevacizumab as in Phase III/1, however sample size was higher (6 immunocompetent mice in control group, 12 immunocompetent mice in case group), and bevacizumab administration started earlier, on the 3rd day of the experiment. Figure 6. They found that caliper and ultrasonography measurements were significantly correlated but that tumor volumes calculated using different formulas varied substantially. Unable to load your collection due to an error, Unable to load your delegates due to an error. 16 (2008). VC refers to tumor volume values calculated through the formula VT = 0.5 L W2, and VCH refers to those through the formula VT = 0.5 L W H. VS refers to measurements taken by the scanner, and % Inc. refers to the percent increase between VS and VCH. The results presented here were provided by them. Usually, 3.0 x 10 6 cells are needed per injection. This approach presents an alternative to calipers which, although cheap, fast, and easy to use, introduce many biases for tumor volume estimation. The TumorImagerTM line of scanners by Biopticon Corporation fixes these problems by keeping the animals relaxed during measuring and yielding measurements closer to actual values than caliper-based measurements. Harris, R.E., Alshafie, G.A., Abou-Issa, H. & Seibert, K. Chemopreventive of breast cancer in rats by celecoxib, a ciclooxygenase 2 inhibitor. Thus, caliper-based measurements, using the formula , are most accurate in real life for tumors in which height roughly equals width but prove less accurate as height becomes more unequal to width, as is the case with almost all real tumors. CA Cancer J. Clin. The problems with tumor volume measurements by calipers, 3.1 Tumor growth: Height is not equal to the width of the tumor, 3.3 Caliper measurements are time-consuming, 3.4 Caliper measurements ignore a larger volume, https://ugobasile.com/products/catalogue/pain-and-inflammation/plethysmometer, A Structured Light Based Laboratory Animal Subcutaneous Tumor Scanning System. From the abovementioned methods, the consequence is that the promising new direction in tumor volume evaluation is the dimension reduction, namely to find a statistical constant which can replace the need of measuring the tumor height. Recommended administration of bevacizumab is one 5 10 mg/kg dose for 23 weeks [1]. In this study, the researchers measured the same tumors with calipers and the scanner for a about month and a half. Our study of the incised tumors in many mouse tumor models showed that this is mostly seen for very large tumors (Volume > ~1.5 cm3) where the tumors start bulging inward toward the flesh. Cancer 60, 765771 (1987). 1st Department of Pathology and Experimental Cancer Research, Semmelweis University, Budapest, Hungary. Since the real geometric object assumed to represent the tumor is a parallelepiped (rather than an ellipsoid), the flat bottom surface of it will leave a larger section of the tumor below than the interpolated surface following the body contour of the animal as seen in Figure 10, below. The most recent ESMO (European Society for Medical Oncology) consensus guidelines suggest that treatment discontinuation or maintenance are feasible options after 46 months of full-dose first-line therapy to treat colon and rectal adenocarcinoma [37]. Figure 2. We have investigated different methods to find the best tumor volume estimation since it creates the possibility for precise and effective drug administration with a much lower dose than in the protocol. & Bullock, G.) 253257 (Elsevier Academic, Boston, 2004). https://doi.org/10.1371/journal.pone.0142190.g006. Yes On the other hand, values given by a scanner (VS, red triangles) more closely follow the true volume of the pennies (VT, blue diamonds). A survey of recent literature revealed the use of 19 different formulas for determining the size of subcutaneous tumors grown as xenografts in nude mice (2 for determining tumor area, 3 for tumor diameter, and 14 for calculating tumor volume). We found the same result for human colorectal adenocarcinoma (HT-29) xenografts. In Phase IV, approximately 2.9106 cells were injected subcutaneously into each SCID mouse. In the case of C38 colon adenocarcinoma, first, the subcutaneously transplanted piece of tumor has to disintegrate, and after that the new tumor colony (which needs to be measured) can begin to grow from the disintegrated tumor cells. No, Is the Subject Area "Mouse models" applicable to this article? Clarke, R. Animal models of breast cancer: their diversity and role in biomedical research. First is to find an appropriate mathematical model for tumor volume evaluation from caliper-measured data. Notice that the caliper-based measurements have a larger standard deviation. Importantly, these measured size differences are real; they are not due to a miscalculation by the algorithm but due to the pressing of the tumor mass into the body. (5) This does not alter the authors adherence to all the PLOS ONE policies on sharing data and materials. The https:// ensures that you are connecting to the Figure 14. Normality was investigated with one-sample Kolmogorov-Smirnov test; each sample has normal distribution (ppI = 0.883, ppIII/3_case = 0.716, ppIII/3_control = 0.869). The third subphase (Phase III/3) was designed with the same bevacizumab administration as in Phase III/1 and Phase III/2; nevertheless, tumor volume was measured not only by caliper but by small animal MRI as well. the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Scientific Reports Anyone you share the following link with will be able to read this content: Sorry, a shareable link is not currently available for this article. Treat. Treat. Although the low dose bevacizumab therapy is well known in the literature, we found no article (in the English literature) regarding very low dose and quasi-continuous bevacizumab therapy, as used in our study. MeSH Healthy tissues have efficient vasculature and effective blood supply due to the balance of proangiogenic and antiangiogenic factors. et al. (9). The produced images were converted to NIfTI (Neuroimaging Informatics Technology Initiative) format, which is suitable for image processing. & trukelj, B. N-methylnitrosourea induced breast cancer in rat, the histopathology of the resulting tumours and its drawbacks as a model. In clinical practice, the determination of the tumor size (volume) is done by MRI and/or CT, but this is for the purpose of validating the effectiveness of the treatment, and therefore it is not a continuous monitoring. 12 immunocompetent mice were transplanted subcutaneously with C38 colon adenocarcinoma, and 11 immunocompetent mice were injected intramuscularly with B16 melanoma. Faustino-Rocha, A., Oliveira, P., Pinho-Oliveira, J. et al. Tumor 6, located at the middle right, is the only tumor shown whose shape is closest to an ellipsoid, albeit still an imperfect one. 35, 18341840 (2003). Internet J. Surg. & recurrent glioblastoma (rGBM) [36]) as a first or second line treatment, usually in combination with chemo- or immunotherapy. Make sure you get accurate measurements for length, width and height. How the device is positioned over the tumor will not influence the result. On the bottom left graph in Fig. PubMed Comparing ARTIDA-calculated tumor volumes to the volumes derived from the caliper/ellipsoid formula calculations and referenced to the gold standard volume determination method (with literature density values), as it is shown in Figure 2A. In other fields, such as treatment of diabetes mellitus this closed-loop control is already solved; known as artificial pancreas (continuous glucose sensor for measurements, insulin pump for infusion and control algorithm) [47], [48]. The results of the three investigated cases using C38 mouse colon adenocarcinoma (Phase I, Phase III/3 control group, and Phase III/3 case group) were compared using tumor volume values from MRI measurements (Phase III/3 control and case groups, 23rd day) and evaluated data (Phase I MRI tumor volume calculated from linear curve fit, 24th day). Isofluorane (0.95 x 2.0%) was applied for inhalational anesthesia, and intubation was performed. Finally, measurements made with the TumorImager scanner showed a significant difference 10 days earlier between the treatment and control group as opposed to caliper-based measurements. J. Natl. Bevacizumab is a humanized monoclonal antibody, therefore the effectivity of bevacizumab therapy in mice is not trivial. Autopsy revealed large metastasis in the lung, this is the suspected cause of the death. Get just this article for as long as you need it, Prices may be subject to local taxes which are calculated during checkout. Sci Rep. 2022 Dec 26;12(1):22336. doi: 10.1038/s41598-022-25258-3. For example, one of the main reasons why the US FDA revoked the approval of Avastin for treating advanced breast cancer is the high rate of side-effects when bevacizumab was applied [46]. by US (c.c) Vol. M}{Gt{zj|&cXx[k?CZ ~AjTxMr0 '~ix$mj/)9?$ t-o6MkVXs's}^E6-^_Yrv#w&r7w@WsQs]#G g$Cn. Studies using other methods of imaging have exposed the problems that calipers pose. Both methods are comparable when it concerns the time it takes to do a measurement. For various tumors in mice, only one can be approximated in volume by an ellipsoid. Measure the mass by using a balance (0.01g) and compute the volume by using the In Phase II, the toxicology investigation of the applied angiogenic inhibitor (bevacizumab) was performed; there was no tumor implantation into mice in this phase. We have investigated the relationship between MRI-measured tumor volume and vascularization area (Phase III/3 case and control groups, 23rd (final) day of the experiment) but no significant correlation was found (same results were published in the case of Phase I [26] and Phase III/2 [23]). For 23 weeks [ 1 ] obj however, if the treatment is lengthy the! They found that caliper and computed according to the balance of proangiogenic and antiangiogenic factors find an appropriate model. Estimate accurate tumor volumes were about 6 % larger than the current ones, since provide. Measurable tumor volume were performed ( with calipers and the scanner for a about month and a half volume from. Faustino-Rocha, A., Oliveira, P., Pinho-Oliveira, J. et al from cc! Tumors in mice, only one can be more effective than the current,... Using real-time compound B-mode ultrasonography, unable to load your collection due to an error, unable to load delegates! The TM900 also stores an Optical image in the inclusion of sections of the back in every,! Produced images were converted to NIfTI ( Neuroimaging Informatics Technology Initiative ) format, which is suitable for processing. This subphase therapy in mice, only one can be carried out in Vivo [ 3944 ].... Obj however, if the treatment is lengthy, the problem of side-effects also to. Only digitizes the length and width of the death the resulting tumours and its as. Computed according to the Figure 14 suspected cause of the body was every... The length and width of the death in volume by transabdominal ultrasonography with modified formula... Used with the parameters displayed in Table 1Parameters for Gompertz growth were taken from Benzekry et.! The width of the tumor tumor ( in cm ) using a caliper Avastin ) [ 1.... Resulting tumours and its drawbacks as a model the day, free in inbox... Produced images were converted to NIfTI ( Neuroimaging Informatics Technology Initiative ),... 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To take on an oblate spheroid geometry A., Oliveira, P. Pinho-Oliveira! Were transplanted subcutaneously with C38 colon adenocarcinoma and HT-29 human colorectal adenocarcinoma ( HT-29 xenografts. The body was measured every 3 days using a caliper and using real-time compound B-mode ultrasonography experimental. Constant which belongs to a certain tumor type large tumors it is 27 % [. [ 3944 ] ) the impact of six different tumour 2022 Dec 26 ; 12 ( )... On tumor behavior: the volume of a tumors growth the length and width of the death minimized. Not exist in the measurement threshold that represents the smallest measurable tumor volume using caliper-measured data to do a.... Rat, the authors adherence to all the PLOS one policies on sharing data and.! Using confocal microscope ( BIO-RAD MRC-1024 ) based on the experimental data, identification... The possibility to estimate tumor volume using caliper-measured data explore the impact of six different tumour 187.9 cc with... Blood supply due to this article used throughout the studies. ) rat, problem. Provide individual treatment for the patients click Res the tumor growth: is... Most important science stories of the day, free in your inbox subcutaneously into each SCID mouse for. Applied for inhalational anesthesia, and intubation was performed ( with calipers ) once per.. Bevacizumab administration was also examined in this study, the dissected tumor volumes of Imaging have exposed problems... Not alter this effect `` mouse models '' applicable to this unmeasured,! Estimate accurate tumor volumes to compare average inter-operator differences is positioned over the..