Differential Rapid Diagnosis of Endometrial Cancer and Its Benign Pathological Conditions Using Surface-Enhanced Raman Spectroscopy

Dmitry N. Artemyev (Login required)
Samara National Research University, Russian Federation

Lyudmila A. Bratchenko
Samara National Research University, Russian Federation

Irina A. Matveeva
Samara National Research University, Russian Federation

Vladimir I. Kukushkin
Institute of Solid State Physics RAS (ISSP RAS), Chernogolovka, Moscow District, Russian Federation

Dmitry Lystsev
First Moscow State Medicine University (Sechenov University), Russian Federation

Anatoly I. Ishchenko
First Moscow State Medicine University (Sechenov University), Russian Federation

Anton A. Ishchenko
First Moscow State Medicine University (Sechenov University), Russian Federation
National Medical Research Center Treatment and Rehabilitation Center, Ministry of Health of the Russian Federation, Moscow, Russian Federation

Vladimir M. Zuev
First Moscow State Medicine University (Sechenov University), Russian Federation

Valery P. Zakharov
Samara National Research University, Russian Federation


Paper #9041 received 24 Nov 2023; revised manuscript received 9 Apr 2024; accepted for publication 19 Apr 2024; published online 7 Jun 2024

DOI: 10.18287/JBPE24.10.020307

Abstract

The purpose of this study is to improve the efficiency of early diagnosis of endometrial cancer using the analysis of surface-enhanced Raman scattering (SERS) of blood plasma. Blood plasma of patients aged 22 to 79 years was investigated. The study included 95 women. All patients were divided into 3 groups: group 1 consists of 29 women with endometrial adenocarcinoma, group 2 − 31 patients with endometrial polyp, group 3 – 10 women with endometrial hyperplasia. A control group consisted of 25 healthy women. The SERS spectra of dried samples were studied on an experimental stand consisting of a Photon-Bio RL785 spectrometric system based on a charge-coupled device (CCD) detector and a laser radiation source with a wavelength of 785 nm and an ADF U300 microscope. In order to realize the effect of surface enhancement of the Raman signal from blood plasma, we used a silver substrate based on a dried silver colloid. In the result of the study, the spectral features and specific features which characteristic of adenocarcinoma, polyps and endometrial hyperplasia were determined. With the use of discriminant analysis by projection onto latent structures (PLS-DA) method, the accuracy of optical diagnostics of endometrial adenocarcinoma relative to the control group and endometrial hyperplasia for the calibration and verification sets of spectra was 87% and 85%, respectively. Class discrimination accuracy of the control group with respect to endometrial hyperplasia and adenocarcinoma was 85%, and endometrial hyperplasia relative to the control group and endometrial adenocarcinoma was 81% for the verification set of spectra. The study shows the possibility of using SERS for differential express diagnostics of endometrial cancer and its benign pathological conditions.

Keywords

blood plasma; polyp; hyperplasia; adenocarcinoma; surface-enhanced Raman spectroscopy; SERS; PLS-DA; projection onto latent structures; discriminant analysis

Full Text:

PDF

References


1. A. N. Sulima, I. O. Kolesnikova, A. A. Davydova, and M. A. Kriventsov, “Hysteroscopic and morphological assessment of intrauterine pathology in different age periods,” Journal of Obstetrics and Women’s Diseases 69(2), 51–58 (2020).

2. V. J. Davis, C. D. Dizon, and C. F. Minuk, “Rare cause of vaginal bleeding in early puberty,” Journal of Pediatric and Adolescent Gynecology 18(2), 113 (2005).

3. S. C. Lee, A. M. Kaunitz, L. Sanchez-Ramos, and R. M. Rhatigan, “The oncogenic potential of endometrial polyps: a systematic review and meta-analysis,” Obstetrics & Gynecology 116(5), 1197–1205 (2010).

4. G. M. Savelyeva, G. T. Sukhikh, V. N. Serov, V. E. Radzinsky, I. B. Manukhin (Eds.), Akusherstvo, 2nd Ed., Geotar-Media, Moscow, (2020). [in Russian].

5. J. V. Jr. Lacey, V. M. Chia, B. B. Rush Danny J. Carreon, Douglas A. Richesson, O. B. Ioffe, B. M. Ronnett, N. Chatterjee, B. Langholz, M. E. Sherman, and A. G. Glass, “Incidence rates of endometrial hyperplasia, endometrial cancer and hysterectomy from 1980 to 2003 within a large prepaid health plan,” International Journal of Cancer 131, 1921–1929 (2012).

6. S. D. Reed, K. M. Newton, W. L. Clinton, M. Epplein, R. Garcia, K. Allison, L. F. Voigt, and N. S. Weiss, “Incidence of endometrial hyperplasia,” American Journal of Obstetrics and Gynecologyl 200(6), 678 (2009).

7. A. D. Kaprin, V. V. Starinsky, A. O. Shakhzadova (Eds.), Malignant neoplasms in Russia in 2020 (morbidity and mortality), MNIOI named after P.A. Herzen – branch of the Federal State Budgetary Institution “National Medical Research Center of Radiology” of the Ministry of Health of Russia, Moscow (2021). [in Russian]. ISBN 978-5-85502-268-1.

8. “Epidemiology of Endometrial Cancer Consortium (E2C2),” National Cancer Institute (accessed 10 October 2019). [https://epi.grants.cancer.gov/eecc/].

9. E. A. Kazachkova, A. V. Zatvornitskaya, E. E. Voropaeva, E. L. Kazachkov, and A. A. Rogozina, “Kliniko-anamnesticheskiye osobennosti i struktura endometriya zhenshchin s giperplaziyey slizistoy obolochki matki v razlichnyye vozrastnyye periody (Clinical and anamnestic features and structure of the endometrium of women with hyperplasia of the uterine mucosa at different age periods),” Ural Medical Journal 150(6), 18–22 (2017). [in Russian].

10. E. N. Polyakova, N. S. Lutsenko, and N. V. Gaidai, “Diagnosis of endometrial hyperplasia in routine gynecological practice,” Zaporozhye Medical Journal 1(112), 95–99 (2019).

11. K. H. Chen, M. J. Pan, Z. Jargalsaikhan, T. O. Ishdorj, and F. G. Tseng, “Development of surface-enhanced raman scattering (sers)-based surface-corrugated nanopillars for biomolecular detection of colorectal cancer,” Biosensors 10(11), 163 (2020).

12. E. Cepeda-Pérez, T. López-Luke, P. Salas, G. Plascencia-Villa, A. Ponce, J. Vivero-Escoto, M. José-Yacamán, and E. de la Rosa, “SERS-active Au/SiO_2 clouds in powder for rapid ex vivo breast adenocarcinoma diagnosis,” Biomedical Optics Express 7(6), 2407 (2016)

13. M. Paraskevaidi, K. M. Ashton, H. F. Stringfellow, N. J. Wood, P. J. Keating, A. W. Rowbottom, P. L. Martin-Hirsch, and F. L. Martin, “Raman spectroscopic techniques to detect ovarian cancer biomarkers in blood plasma,” Talanta 189, 281–288 (2018).

14. S. Li, L. Li, Q. Zeng, Y. Zhang, Z. Guo, Z. Liu, M. Jin, C. Su, L. Lin, J. Xu, and S. Liu, “Characterization and noninvasive diagnosis of bladder cancer with serum surface enhanced raman spectroscopy and genetic algorithms,” Scientific Reports 5, 1–7 (2015).

15. D. N. Artemyev, V. I. Kukushkin, S. T. Avraamova, N. S. Aleksandrov, and Y. A. Kirillov, “Using the method of "optical biopsy" of prostatic tissue to diagnose prostate cancer,” Molecules 26(7), 1961 (2021).

16. J. Depciuch, E. Barnaś, J. Skręt-Magierło, A. Skręt, E. Kaznowska, K. Łach, P. Jakubczyk, and J. Cebulski, “Spectroscopic evaluation of carcinogenesis in endometrial cancer,” Scientific Reports 11, 9079 (2021).

17. S. Z. Al-Sammarraie, L. A. Bratchenko, E. N. Typikova, V. P. Zakharov, I. A. Bratchenko, and P. A. Lebedev, “Silver nanoparticles-based substrate for blood serum analysis under 785 nm laser excitation Journal of Biomedical Photonics & Engineering 8(1), 010301 (2022).

18. A. Savitzky, M. Golay, “Smoothing and differentiation of data by simplified least squares procedures,” Analytical Chemistry, 36(8), 1627−1639 (1964).

19. S. J. Baek, A. Park, Y. J. Ahn, and J. Choo, “Baseline correction using asymmetrically reweighted penalized least squares smoothing,” Analyst 140(1), 250–257 (2015).

20. M. Tahira, H. Nawaz, M. I. Majeed, N. Rashid, S. Tabbasum, M. Abubakar, S. Ahmad, S. Akbar, S. Bashir, M. Kashif, S. Ali, and H. Hyat, “Surface-enhanced Raman spectroscopy analysis of serum samples of typhoid patients of different stages,” Photodiagnosis and Photodynamic Therapy 34, 102329 (2021).

21. S. Feng, W. Wang, I. T. Tai, G. Chen, R. Chen, and H. Zeng, “Label-free surface-enhanced Raman spectroscopy for detection of colorectal cancer and precursor lesions using blood plasma,” Biomedical Optics Express 6(9), 3494–3502 (2015).

22. L. A. Bratchenko, S. Z. Al-Sammarraie, E. N. Tupikova, D. Y. Konovalova, P. A. Lebedev, V. P. Zakharov, and I. A. Bratchenko, “Analyzing the serum of hemodialysis patients with end-stage chronic kidney disease by means of the combination of SERS and machine learning,” Biomedical Optics Express 3(9), 4926–4938 (2022).

23. S. De Jong, “SIMPLS: an alternative approach to partial least squares regression,” Chemometrics and Intelligent Laboratory Systems 18(3), 251–263 (1993).

24. F. S. Nahm, “Receiver operating characteristic curve: overview and practical use for clinicians,” Korean Journal of Anesthesiology 75(1), 25−36 (2022).

25. S. Rubina, C. M. Krishna, “Raman spectroscopy in cervical cancers: An update,” Journal of Cancer Research and Therapeutics 11(1), 10–17 (2015).

26. U. Parlatan, M. T. Inanc, B. Y. Ozgor, E. Oral, E. Bastu, M. B. Unlu, and G. Basar, “Raman spectroscopy as a non-invasive diagnostic technique for endometriosis,” Scientific Reports 9(1), 19795 (2019).

27. E. Barnas, J. Skret-Magierlo, A. Skret, E. Kaznowska, J. Depciuch, K. Szmuc, K. Łach, I. Krawczyk-Marć, and J. Cebulski, “Simultaneous FTIR and Raman spectroscopy in endometrial atypical hyperplasia and cancer,” International Journal of Molecular Sciences 21(14), 4828 (2020).

28. S. Feng, R. Chen, J. Lin, J. Pan, Y. Wu, Y. Li, J. Chen, and H. Zeng, “Gastric cancer detection based on blood plasma surface-enhanced Raman spectroscopy excited by polarized laser light,” Biosensors and Bioelectronics 26(7), 3167–3174 (2011).

29. S. Feng, R. Chen, J. Lin, J. Pan, G. Chen, Y. Li, M. Cheng, Z. Huang, J. Chen, and H. Zeng, “Nasopharyngeal cancer detection based on blood plasma surface-enhanced Raman spectroscopy and multivariate analysis,” Biosensors and Bioelectronics 25(11), 2414–9 (2010).

30. H. Qian, Y. Wang, Z. Ma, L. Qian, X. Shao, D. Jin, M. Cao, S. Liu, H. Chen, J. Pan, and W. Xue, “Surface-enhanced raman spectroscopy of pretreated plasma samples predicts disease recurrence in muscle-invasive bladder cancer patients undergoing neoadjuvant chemotherapy and radical cystectomy,” International Journal of Nanomedicine 17, 1635–1646 (2022).

31. A. Bonifacio, S. D. Marta, R. Spizzo, S. Cervo, A. Steffan, A. Colombatti, and V. Sergo, “Surface-enhanced Raman spectroscopy of blood plasma and serum using Ag and Au nanoparticles: a systematic study,” Analytical and Bioanalytical Chemistry 406(9–10), 2355–2365 (2014).

32. Z. Movasaghi, S. Rehman, and I. U. Rehman, “Raman spectroscopy of biological tissues,” Applied Spectroscopy Reviews 42(5), 493–541 (2007).

33. M. Paraskevaidi, K. M. Ashton, H. F. Stringfellow, N. J. Wood, P. J. Keating, A. W. Rowbottom, P. L. Martin-Hirsch, and F. L. Martin, “Raman spectroscopic techniques to detect ovarian cancer biomarkers in blood plasma,” Talanta 189, 281–288 (2018).

34. J. De Gelder, K. De Gussem, P. Vandenabeele, and L. Moens, “Reference database of Raman spectra of biological molecules,” International Journal for Original Work in all Aspects of Raman Spectroscopy, Including Higher Order Processes, and also Brillouin and Rayleigh Scattering 38(9), 1133–1147 (2007).

35. B. Hernández, F. Pflüger, S. G. Kruglik, and M. Ghomi, “Characteristic raman lines of phenylalanine analyzed by a multiconformational approach,” Journal of Raman Spectroscopy 44, 827–833 (2013).

36. H. Song, J. S. Peng, Y. Dong-Sheng, Z. L. Yang, H. L. Liu, Y. K. Zeng, X. P. Shi, and B. Y. Lu, “Serum metabolic profiling of human gastric cancer based on gas chromatography/mass spectrometry,” Brazilian Journal of Medical and Biological Research 45(1), 78–85 (2012).

37. M. Paraskevaidi, C. L. M. Morais, K. M. Ashton, H. F. Stringfellow, R. J. McVey, N. A. J. Ryan, H. O’Flynn, V. N. Sivalingam, S. J. Kitson, M. L. MacKintosh, A. E. Derbyshire, C. Pow, O. Raglan, K. M. G. Lima, M. Kyrgiou, P. L. Martin-Hirsch, F. L. Martin, and E. J. Crosbie, “Detecting Endometrial Cancer by Blood Spectroscopy: A Diagnostic Cross-Sectional Study,” Cancers 12(5), 1256 (2020).






© 2014-2024 Samara National Research University. All Rights Reserved.
Public Media Certificate (RUS). 12+