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Association between Chromatin Structural Organization of Peripheral Blood Neutrophils and Self-Perceived Mental Stress: Gray-Level Co-occurrence Matrix Analysis

Published online by Cambridge University Press:  02 August 2021

Nikola Topalovic ,
Sanja Mazic ,
Dejan Nesic ,
Olivera Vukovic ,
Jelena Cumic ,
Darko Laketic ,
Ivana Stasevic Karlicic  and
Igor Pantic Open the ORCID record for Igor Pantic [Opens in a new window]
Nikola Topalovic
Affiliation:
University of Belgrade, Faculty of Medicine, Institute of Medical Physiology, Visegradska 26/II, RS-11129, Belgrade, Serbia
Sanja Mazic
Affiliation:
University of Belgrade, Faculty of Medicine, Institute of Medical Physiology, Visegradska 26/II, RS-11129, Belgrade, Serbia
Dejan Nesic
Affiliation:
University of Belgrade, Faculty of Medicine, Institute of Medical Physiology, Visegradska 26/II, RS-11129, Belgrade, Serbia
Olivera Vukovic
Affiliation:
University of Belgrade, Faculty of Medicine, Institute of Mental Health, Palmoticeva 37, RS-11000, Belgrade, Serbia
Jelena Cumic
Affiliation:
University of Belgrade, Faculty of Medicine, University Clinical Centre of Serbia, Dr. Koste Todorovica 8, RS-11129, Belgrade, Serbia
Darko Laketic
Affiliation:
University of Belgrade, Faculty of Medicine, Institute of Anatomy, Dr Subotica 4/2, RS-11129, Belgrade, Serbia
Ivana Stasevic Karlicic
Affiliation:
Clinic for Mental Disorders Dr Laza Lazarevic, Visegradska 26, RS-11129, Belgrade, Serbia
Igor Pantic*
Affiliation:
University of Belgrade, Faculty of Medicine, Institute of Medical Physiology, Visegradska 26/II, RS-11129, Belgrade, Serbia University of Haifa, 199 Abba Hushi Blvd. Mount Carmel, HaifaIL-3498838, Israel
*
*Corresponding author: Igor Pantic, E-mail: [email protected]; [email protected]
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Abstract

Methods based on the evaluation of textural patterns in microscopy, such as the “gray-level co-occurrence matrix” (GLCM) analysis are modern and innovative computer and mathematical algorithms that can be used to quantify subtle structural changes in cells and their organelles. Potential application of GLCM method in the fields of psychophysiology and psychiatry to this date has not been systematically investigated. The main objective of our study was to test the existence and strength of the association between chromatin structural organization of peripheral blood neutrophils and levels of self-perceived mental stress. The research was done on a sample of 100 healthy student athletes, and the Depression, Anxiety, and Stress Scales (DASS-21) were used for the estimation of psychological distress. Chromatin textural homogeneity and uniformity were negatively correlated (p < 0.01) with mental distress and had relatively good discriminatory power in differentiating participants with normal and elevated stress levels. As an addition, we propose the creation of a machine learning model based on binomial logistic regression that uses these and other GLCM features to predict stress elevation. To the best of our knowledge, these results are one of the first to establish the link between neutrophil chromatin structural organization quantified by the GLCM method and indicators of normal psychological functioning.

Keywords

microscopymorphologyneutrophilnucleustexture
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 27 , Issue 5 , October 2021 , pp. 1202 - 1208
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the Microscopy Society of America

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References

Beaufort, IN, De Weert-Van Oene, GH, Buwalda, VAJ, de Leeuw, JRJ & Goudriaan, AE (2017). The depression, anxiety and stress scale (DASS-21) as a screener for depression in substance use disorder inpatients: A pilot study. Eur Addict Res 23(5), 260–268.CrossRefGoogle ScholarPubMed
Biran, A, Zada, L, Abou Karam, P, Vadai, E, Roitman, L, Ovadya, Y, Porat, Z & Krizhanovsky, V (2017). Quantitative identification of senescent cells in aging and disease. Aging Cell 16(4), 661–671.CrossRefGoogle ScholarPubMed
Blachnio, A, Przepiorka, A & Pantic, I (2015). Internet use, facebook intrusion, and depression: Results of a cross-sectional study. Eur Psychiatry 30(6), 681–684.CrossRefGoogle ScholarPubMed
Chang, MC & Mrkonjic, M (2020). Review of the current state of digital image analysis in breast pathology. Breast J 26(6), 1208–1212.CrossRefGoogle ScholarPubMed
Davidovic, LM, Laketic, D, Cumic, J, Jordanova, E & Pantic, I (2021). Application of artificial intelligence for detection of chemico-biological interactions associated with oxidative stress and DNA damage. Chem Biol Interact 345, 109533.CrossRefGoogle ScholarPubMed
Demir, S, Atli, A, Bulut, M, Ibiloglu, AO, Gunes, M, Kaya, MC, Demirpence, O & Sir, A (2015). Neutrophil-lymphocyte ratio in patients with major depressive disorder undergoing no pharmacological therapy. Neuropsychiatr Dis Treat 11, 2253–2258.Google ScholarPubMed
Dhruv, B, Mittal, N & Modi, M (2019). Study of Haralick's and GLCM texture analysis on 3D medical images. Int J Neurosci 129(4), 350–362.CrossRefGoogle ScholarPubMed
Dincic, M, Todorovic, J, Nesovic Ostojic, J, Kovacevic, S, Dunderovic, D, Lopicic, S, Spasic, S, Radojevic-Skodric, S, Stanisavljevic, D & Ilic, AZ (2020). The fractal and GLCM textural parameters of chromatin may be potential biomarkers of papillary thyroid carcinoma in hashimoto's thyroiditis specimens. Microsc Microanal 26(4), 717–730.CrossRefGoogle ScholarPubMed
El-Benna, J, Hurtado-Nedelec, M, Marzaioli, V, Marie, JC, Gougerot-Pocidalo, MA & Dang, PM (2016). Priming of the neutrophil respiratory burst: Role in host defense and inflammation. Immunol Rev 273(1), 180–193.CrossRefGoogle ScholarPubMed
Faith, RE, Murgo, AJ, Good, RA & Plotnikoff, NP (2019). Cytokines, Stress and Immunity, 2nd ed. Boca Raton, FL, USA: CRC Press, Taylor & Francis.Google Scholar
Fatima, K, Naqvi, F & Younas, H (2021). A review: Molecular chaperone-mediated folding, unfolding and disaggregation of expressed recombinant proteins. Cell Biochem Biophys 79(2), 153–174.CrossRefGoogle ScholarPubMed
Hayashi, T (2015). Conversion of psychological stress into cellular stress response: Roles of the sigma-1 receptor in the process. Psychiatry Clin Neurosci 69(4), 179–191.CrossRefGoogle ScholarPubMed
Houtepen, LC, Vinkers, CH, Carrillo-Roa, T, Hiemstra, M, van Lier, PA, Meeus, W, Branje, S, Heim, CM, Nemeroff, CB, Mill, J, Schalkwyk, LC, Creyghton, MP, Kahn, RS, Joels, M, Binder, EB & Boks, MP (2016). Genome-wide DNA methylation levels and altered cortisol stress reactivity following childhood trauma in humans. Nat Commun 7, 10967.CrossRefGoogle ScholarPubMed
Hu, J, Qian, W, Yu, Z, Xu, T, Ju, L, Hua, Q, Wang, Y, Ling, JJ & Lv, H (2020). Increased neutrophil respiratory burst predicts the risk of coronary artery lesion in kawasaki disease. Front Pediatr 8, 391.CrossRefGoogle ScholarPubMed
Jiang, S, Postovit, L, Cattaneo, A, Binder, EB & Aitchison, KJ (2019). Epigenetic modifications in stress response genes associated with childhood trauma. Front Psychiatry 10, 808.CrossRefGoogle ScholarPubMed
Khanfer, R, Phillips, AC, Carroll, D & Lord, JM (2010). Altered human neutrophil function in response to acute psychological stress. Psychosom Med 72(7), 636–640.CrossRefGoogle ScholarPubMed
Kinoshita, M, Nakashima, H, Nakashima, M, Koga, M, Toda, H, Koiwai, K, Morimoto, Y, Miyazaki, H, Saitoh, D, Suzuki, H & Seki, S (2019). The reduced bactericidal activity of neutrophils as an incisive indicator of water-immersion restraint stress and impaired exercise performance in mice. Sci Rep 9(1), 4562.CrossRefGoogle ScholarPubMed
Lee, D (2019). The convergent, discriminant, and nomological validity of the Depression Anxiety Stress Scales-21 (DASS-21). J Affect Disord 259, 136–142.CrossRefGoogle Scholar
Lord, JM, Phillips, AC & Arlt, W (2019). Synergistic Effects of Aging and Stress on Neutrophil Function. Cham, Berlin: Springer.CrossRefGoogle Scholar
Lovibond, SH & Lovibond, PF (1995). Manual for the Depression Anxiety Stress Scales, 2nd ed. Sydney, Australia: Psychology Foundation.Google Scholar
Miyazaki, H, Kinoshita, M, Ono, S, Seki, S & Saitoh, D (2015). Burn-evoked reactive oxygen species immediately after injury are crucial to restore the neutrophil function against postburn infection in mice. Shock 44(3), 252–257.CrossRefGoogle ScholarPubMed
Nikolovski, D, Cumic, J & Pantic, I (2019). Application of gray level co-occurrence matrix algorithm for detection of discrete structural changes in cell nuclei after exposure to iron oxide nanoparticles and 6-hydroxydopamine. Microsc Microanal 25(4), 982–988.CrossRefGoogle ScholarPubMed
Pantic, I, Cumic, J, Skodric, SR, Dugalic, S & Brodski, C (2021). Oxidopamine and oxidative stress: Recent advances in experimental physiology and pharmacology. Chem Biol Interact 336, 109380.CrossRefGoogle ScholarPubMed
Pantic, I, Dacic, S, Brkic, P, Lavrnja, I, Jovanovic, T, Pantic, S & Pekovic, S (2015). Discriminatory ability of fractal and grey level co-occurrence matrix methods in structural analysis of hippocampus layers. J Theor Biol 370, 151–156.CrossRefGoogle ScholarPubMed
Pantic, I, Dacic, S, Brkic, P, Lavrnja, I, Pantic, S, Jovanovic, T & Pekovic, S (2014). Application of fractal and grey level co-occurrence matrix analysis in evaluation of brain corpus callosum and cingulum architecture. Microsc Microanal 20(5), 1373–1381.CrossRefGoogle ScholarPubMed
Pantic, I, Dimitrijevic, D, Nesic, D & Petrovic, D (2016a). Gray level co-occurrence matrix algorithm as pattern recognition biosensor for oxidopamine-induced changes in lymphocyte chromatin architecture. J Theor Biol 406, 124–128.CrossRefGoogle Scholar
Pantic, I, Dimitrijevic, D, Stasevic-Karlicic, I, Jeremic, M, Starcevic, A, Ristic, S, Blachnio, A & Przepiorka, A (2019). Chromatin textural parameters of blood neutrophils are associated with stress levels in patients with recurrent depressive disorder. Srp Arh Za Celok Lek 147(11–12), 718–723.CrossRefGoogle Scholar
Pantic, I, Jeremic, R, Dacic, S, Pekovic, S, Pantic, S, Djelic, M, Vitic, Z, Brkic, P & Brodski, C (2020). Gray-level co-occurrence matrix analysis of granule neurons of the hippocampal dentate gyrus following cortical injury. Microsc Microanal 26(1), 166–172.CrossRefGoogle ScholarPubMed
Pantic, I, Milanovic, A, Loboda, B, Blachnio, A, Przepiorka, A, Nesic, D, Mazic, S, Dugalic, S & Ristic, S (2017). Association between physiological oscillations in self-esteem, narcissism and internet addiction: A cross-sectional study. Psychiatry Res 258, 239–243.CrossRefGoogle ScholarPubMed
Pantic, I, Nesic, D, Basailovic, M, Cetkovic, M, Mazic, S, Suzic-Lazic, J & Popevic, M (2016b). Chromatin fractal organization, textural patterns, and circularity of nuclear envelope in adrenal zona Fasciculata cells. Microsc Microanal 22(6), 1120–1127.CrossRefGoogle Scholar
Pantic, I, Pantic, S & Paunovic, J (2012). Aging increases nuclear chromatin entropy of erythroid precursor cells in mice spleen hematopoietic tissue. Microsc Microanal 18(5), 1054–1059.CrossRefGoogle ScholarPubMed
Paunovic, J, Vucevic, D, Radosavljevic, T, Mandic-Rajcevic, S & Pantic, I (2020). Iron-based nanoparticles and their potential toxicity: Focus on oxidative stress and apoptosis. Chem Biol Interact 316, 108935.CrossRefGoogle ScholarPubMed
Petrovic, D, Perovic, M, Lazovic, B & Pantic, I (2016). Association between walking, dysphoric mood and anxiety in late pregnancy: A cross-sectional study. Psychiatry Res 246, 360–363.CrossRefGoogle ScholarPubMed
Roufayel, R & Kadry, S (2019). Molecular chaperone HSP70 and key regulators of apoptosis: A review. Curr Mol Med 19(5), 315–325.CrossRefGoogle ScholarPubMed
Salinas, C, Espinosa, G, Morales, N, Henriquez, C, Moran, G, Gajardo, G & Uberti, B (2020). Assessment of peripheral blood neutrophil respiratory burst, phagocytosis and apoptosis in obese non-insulin dysregulated horses. Res Vet Sci 132, 127–132.CrossRefGoogle ScholarPubMed
Scholten, S, Velten, J, Bieda, A, Zhang, XC & Margraf, J (2017). Testing measurement invariance of the Depression, Anxiety, and Stress Scales (DASS-21) across four countries. Psychol Assess 29(11), 1376–1390.CrossRefGoogle ScholarPubMed
Tan, TC, Ritter, LJ, Whitty, A, Fernandez, RC, Moran, LJ, Robertson, SA, Thompson, JG & Brown, HM (2016). Gray level co-occurrence matrices (GLCM) to assess microstructural and textural changes in pre-implantation embryos. Mol Reprod Dev 83(8), 701–713.CrossRefGoogle ScholarPubMed
Thakur, N, Yoon, H & Chong, Y (2020). Current trends of artificial intelligence for colorectal cancer pathology image analysis: A systematic review. Cancers 12, 7.CrossRefGoogle ScholarPubMed
Tsukamoto, K & Machida, K (2014). Effects of psychological stress on neutrophil phagocytosis and bactericidal activity in humans: A meta-analysis. Int J Psychophysiol 91(2), 67–72.CrossRefGoogle ScholarPubMed
Turk, F & Waller, G (2020). Is self-compassion relevant to the pathology and treatment of eating and body image concerns? A systematic review and meta-analysis. Clin Psychol Rev 79, 101856.CrossRefGoogle ScholarPubMed