The morphofunctional state of the fetal thyroid gland in maternal-fetal infections caused by Escherichia coli, Staphylococcus aureus and Klebsiella pneumoniae

Authors

DOI:

https://doi.org/10.14739/2310-1237.2021.1.216292

Keywords:

thyroid gland, fetus, rats Wistar, Escherichia coli, Staphylococcus aureus, Klebsiella pneumoniae, maternal-fetal exchange, pregnancy complications, infectious

Abstract

Aim experimental modelling and determination of the morphofunctional state of the thyroid gland of a rat fetus in maternal-fetal infections caused by E. coli, S. aureus and K. pneumoniae.

Material and methods. We conducted a controlled experimental study with block randomization on 85 female Wistar Albino Glaxo rats, which, depending on the group assigned randomly, were infected or not with E. coli, S. aureus and K. pneumoniae before pregnancy with subsequent pathomorphological examination of 37 thyroid glands obtained from rats’ fetuses. The set of methods was applied: histological – HE and Mallory staining; indirect immunofluorescence: moAb to T4, types I and III collagen, IL-6, and TNF; histomorphometry using ImageJ software. Statistical analysis was performed with the R environment and packages “ggplot”, “dplyr”, “pastecs”, “graphics” for Shapiro–Wilk test, Bartlett’s test, Box-Cox method, ANOVA, and plotting. The null hypothesis was rejected in cases when an error probability (P) did not exceed the type I error set at 0.001 (P < 0.001).

Results. In the thyroid glands of fetuses obtained from mothers infected with E. coli, S. aureus and K. pneumoniae, in comparison with the control group, a statistically significant increase in the following morphofunctional parameters was determined: the diameter and area of the follicle, the area of the colloid, the height and area of the thyrocyte, the intensity and area of the fluorescence of the follicular thyrocytes and colloid, in samples labeled MoAb to T4, the intensity of the fluorescence of collagen types I and III; a decrease in the area of the nucleus in relation to the area of the cytoplasm, which was reflected in a decrease in the NCR index. The most pronounced differences in morphological and functional parameters from the norm were found in the thyroid gland of fetuses from mothers infected with S. aureus.

Conclusions. The revealed changes in the morphofunctional parameters of the thyroid gland of a rat fetus, which experienced the influence of maternal-fetal infections caused by E. coli, S. aureus and K. pneumoniae, are unidirectional and statistically significantly different from those recorded during physiological organogenesis. They correspond to an increase in the gland’s secretory activity and indicate the acceleration of organ’s maturation.

Author Biographies

P. S. Talapova, Kharkiv National Medical University, Ukraine

PhD student of the Department of Pathological Anatomy

I. V. Sorokina, Kharkiv National Medical University, Ukraine

MD, PhD, DSc, Professor of the Department of Pathological Anatomy

References

Harmon, Q. E., Basso, O., Weinberg, C. R., & Wilcox, A. J. (2018). Two denominators for one numerator: the example of neonatal mortality. European journal of epidemiology, 33(6), 523-530. https://doi.org/10.1007/s10654-018-0373-0

Neu, N., Duchon, J., & Zachariah, P. (2015). TORCH infections. Clinics in perinatology, 42(1), 77-103. https://doi.org/10.1016/j.clp.2014.11.001

Singh, M., Alsaleem, M., & Gray, C. P. (2021). Neonatal Sepsis. In StatPearls. StatPearls Publishing. https://www.ncbi.nlm.nih.gov/books/NBK531478/

Doster, R. S., Kirk, L. A., Tetz, L. M., Rogers, L. M., Aronoff, D. M., & Gaddy, J. A. (2017). Staphylococcus aureus Infection of Human Gestational Membranes Induces Bacterial Biofilm Formation and Host Production of Cytokines. The Journal of infectious diseases, 215(4), 653-657. https://doi.org/10.1093/infdis/jiw300

Bonasoni, M. P., Palicelli, A., Dalla Dea, G., Comitini, G., Nardini, P., Vizzini, L., Russello, G., Bardaro, M., & Carretto, E. (2021). Klebsiella pneumoniae Chorioamnionitis: An Underrecognized Cause of Preterm Premature Rupture of Membranes in the Second Trimester. Microorganisms, 9(1), 96. https://doi.org/10.3390/microorganisms9010096

Vakili, S., Savardashtaki, A., Jamalnia, S., Tabrizi, R., Nematollahi, M. H., Jafarinia, M., & Akbari, H. (2020). Laboratory Findings of COVID-19 Infection are Conflicting in Different Age Groups and Pregnant Women: A Literature Review. Archives of medical research, 51(7), 603-607. https://doi.org/10.1016/j.arcmed.2020.06.007

Liu, H., Wang, L. L., Zhao, S. J., Kwak-Kim, J., Mor, G., & Liao, A. H. (2020). Why are pregnant women susceptible to COVID-19? An immunological viewpoint. Journal of reproductive immunology, 139, 103122. https://doi.org/10.1016/j.jri.2020.103122

Avni, T., Babitch, T., Ben-Zvi, H., Hijazi, R., Ayada, G., Atamna, A., & Bishara, J. (2020). Clostridioides difficile infection in immunocompromised hospitalized patients is associated with a high recurrence rate. International journal of infectious diseases : IJID, 90, 237-242. https://doi.org/10.1016/j.ijid.2019.10.028

Bajaj, S. K., & Tombach, B. (2017). Respiratory infections in immunocompromised patients: Lung findings using chest computed tomography. Radiology of infectious diseases, 4(1), 29-37. https://doi.org/10.1016/j.jrid.2016.11.001

Markovskiy, V. D., & Sakal, A. A. (2016). Morfofunktsional'noe sostoyanie pecheni potomstva ot materei, infitsirovannykh Esherichia Coli (eksperimental'noe issledovanie) [Morphofunctional state of the liver of rat progeny from mothers, infected with Esherichia Coli (experimental research)]. Morphologia, 10(3), 199-202. [in Russian].

Sorokina, I. V., Myroshnychenko, M. S., & Ivanova, M. D. (2018). Morfologicheskie osobennosti pochek plodov i novorozhdennykh ot materei s podostrym infektsionno-vospalitel'nym protsessom v bryushnoi polosti, vyzvannym Escherichia coli (eksperimental'noe issledovanie) [Morphological features of kidneys in fetuses and newborns from mothers with subacute infectious-inflammatory process in the abdominal cavity caused by Escherichia coli (experimental study)]. Pochki - Kidneys, 7(1), 18-25. [in Russian]. https://doi.org/10.22141/2307-1257.7.1.2018.122216

Tovazhnianska, V. D., Sorokina, I. V., Yakovtsova, & I. I. (2016). Vliyanie materinskogo klebsielleza na morfofunktsional'noe sostoyanie kory nadpochechnikov plodov (eksperimental'noe issledovanie) [Influence of maternal infection caused by Klebsiella pneumonia on morphologic and functional state of fetuses’ adrenal glands cortex (experimental research)]. Morphologia, 10(3), 283-287. [in Russian].

Churilov, L. P., Sobolevskaia, P. A., & Stroev, Y. I. (2019). Thyroid gland and brain: Enigma of Hashimoto's encephalopathy. Best practice & research. Clinical endocrinology & metabolism, 33(6), 101364. https://doi.org/10.1016/j.beem.2019.101364

Bronchain, O. J., Chesneau, A., Monsoro-Burq, A. H., Jolivet, P., Paillard, E., Scanlan, T. S., Demeneix, B. A., Sachs, L. M., & Pollet, N. (2017). Implication of thyroid hormone signaling in neural crest cells migration: Evidence from thyroid hormone receptor beta knockdown and NH3 antagonist studies. Molecular and cellular endocrinology, 439, 233-246. https://doi.org/10.1016/j.mce.2016.09.007

Yaglova, N. V., Sledneva, Y. P., & Yaglov, V. V. (2016). Morphofunctional Changes in the Thyroid Gland of Pubertal and Postpubertal Rats Exposed to Low Dose of DDT. Bulletin of experimental biology and medicine, 162(2), 260-263. https://doi.org/10.1007/s10517-016-3590-0

Yanko, R., Levashov, M., Chaka, E., Litovka, I., & Safonov, S. (2020). Seasonal features of the combined effects of intermittent normobabic hypoxia and melatonin on the thyroid gland morphofunctional state. Journal of Education, Health and Sport, 10(4), 186-198. http://dx.doi.org/10.12775/JEHS.2020.10.04.021

Owji, M. S., Varedi, M., Naghibalhossaini, F., & Pajouhi, N. (2020). Thyroid Function Modulates Lung Fluid and Alveolar Viscoelasticity in Mechanically Ventilated Rat. The Journal of surgical research, 253, 272-279. https://doi.org/10.1016/j.jss.2020.03.060

Yoshimi, K., & Mashimo, T. (2018). Application of genome editing technologies in rats for human disease models. Journal of human genetics, 63(2), 115-123. https://doi.org/10.1038/s10038-017-0346-2

Hashway, S. A., & Wilding, L. A. (2019). Benefits of Rat Models. In M. A. Suckow, R. P. Wilson, F. C. Hankenson, & P. L. Foley (Eds.), The laboratory Rat (pp. 77-79). Academic Press. https://doi.org/10.1016/C2017-0-01188-6

Xia, T., Zhang, X., Wang, Y., & Deng, D. (2018). Effect of maternal hypothyroidism during pregnancy on insulin resistance, lipid accumulation, and mitochondrial dysfunction in skeletal muscle of fetal rats. Bioscience reports, 38(4), BSR20171731. https://doi.org/10.1042/BSR20171731

Markovskyi, V. D., Sorokіna, І. V., Miroshnychenko, M. S., Plіten O. M., Mіshyna M. M., Shapkіn A. S., & Kaluzhyna, O. V. (2015). Sposib modeliuvannia vnutrishnoutrobnoho infikuvannia ploda ta novonarodzhenoho yak naslidku pidhostroho infektsiino-zapalnoho protsesu materi [Method for modeling intrauterine infection of fetus and newborn as a consequence of sub-acute infectious-inflammatory mother process]. Ukraine Patent UA 108806. https://uapatents.com/7-108806-sposib-modelyuvannya-vnutrishnoutrobnogo-infikuvannya-ploda-ta-novonarodzhenogo-yak-naslidku-pidgostrogo-infekcijjno-zapalnogo-procesu-materi.html

Razavi, M. A., Wong, J., Akkera, M., Shalaby, M., Shalaby, H., Sholl, A., Haddad, A., Behl, P., Kandil, E., & Lee, G. S. (2020). Nuclear morphometry in indeterminate thyroid nodules. Gland surgery, 9(2), 238-244. https://doi.org/10.21037/gs.2020.02.02

Schindelin, J., Rueden, C. T., Hiner, M. C., & Eliceiri, K. W. (2015). The ImageJ ecosystem: An open platform for biomedical image analysis. Molecular reproduction and development, 82(7-8), 518-529. https://doi.org/10.1002/mrd.22489

Gao, D., Barber, P. R., Chacko, J. V., Kader Sagar, M. A., Rueden, C. T., Grislis, A. R., Hiner, M. C., & Eliceiri, K. W. (2020). FLIMJ: An open-source ImageJ toolkit for fluorescence lifetime image data analysis. PloS one, 15(12), e0238327. https://doi.org/10.1371/journal.pone.0238327

Labno, C. (2019). Basic Intensity Quantification with ImageJ. Integrated Light Microscopy Core, University of Chicago. https://www.unige.ch/medecine/bioimaging/files/1914/1208/6000/Quantification.pdf

Pereira, D., Richert, A., Medjkane, S., Hénon, S., & Weitzman, J. B. (2020). Cell geometry and the cytoskeleton impact the nucleo-cytoplasmic localisation of the SMYD3 methyltransferase. Scientific reports, 10(1), 20598. https://doi.org/10.1038/s41598-020-75833-9

Liu J. (2020). The "life code": A theory that unifies the human life cycle and the origin of human tumors. Seminars in cancer biology, 60, 380-397. https://doi.org/10.1016/j.semcancer.2019.09.005

Smelova, I. V., & Golovneva, E. S. (2018). Izuchenie morfofunktsional'nykh izmenenii follikulov shchitovidnoi zhelezy krys v norme i pri gipotireoze posle vozdeistviya sredneintensivnogo lazernogo izlucheniya [The study of morphological and functional changes in the thyroid follicles of healthy rats and rats with experimentally induced hypothyroidism following exposure to medium-power laser radiation]. Bulletin of RSMU, (3), 65-71. [in Russian]. https://doi.org/10.24075/brsmu.2018.028

Nilsson, M., & Fagman, H. (2017). Development of the thyroid gland. Development, 144(12), 2123-2140. https://doi.org/10.1242/dev.145615

Van der Spek, A. H., Surovtseva, O. V., Jim, K. K., van Oudenaren, A., Brouwer, M. C., Vandenbroucke-Grauls, C., Leenen, P., van de Beek, D., Hernandez, A., Fliers, E., & Boelen, A. (2018). Regulation of Intracellular Triiodothyronine Is Essential for Optimal Macrophage Function. Endocrinology, 159(5), 2241-2252. https://doi.org/10.1210/en.2018-00053

Fröhlich, E., & Wahl, R. (2019). Microbiota and Thyroid Interaction in Health and Disease. Trends in endocrinology and metabolism: TEM, 30(8), 479-490. https://doi.org/10.1016/j.tem.2019.05.008

Asgari, M., Latifi, N., Heris, H. K., Vali, H., & Mongeau, L. (2017). In vitro fibrillogenesis of tropocollagen type III in collagen type I affects its relative fibrillar topology and mechanics. Scientific reports, 7(1), 1392. https://doi.org/10.1038/s41598-017-01476-y

Mancini, A., Di Segni, C., Raimondo, S., Olivieri, G., Silvestrini, A., Meucci, E., & Currò, D. (2016). Thyroid Hormones, Oxidative Stress, and Inflammation. Mediators of inflammation, 2016, 6757154. https://doi.org/10.1155/2016/6757154

Paschou, S. A., Palioura, E., Kothonas, F., Myroforidis, A., Loi, V., Poulou, A., Goumas, K., Effraimidis, G., & Vryonidou, A. (2018). The effect of anti-TNF therapy on thyroid function in patients with inflammatory bowel disease. Endocrine journal, 65(11), 1121-1125. https://doi.org/10.1507/endocrj.EJ18-0243

Rubingh, J., van der Spek, A., Fliers, E., & Boelen, A. (2020). The Role of Thyroid Hormone in the Innate and Adaptive Immune Response during Infection. Comprehensive Physiology, 10(4), 1277-1287. https://doi.org/10.1002/cphy.c200003

Published

2021-05-18

How to Cite

1.
Talapova PS, Sorokina IV. The morphofunctional state of the fetal thyroid gland in maternal-fetal infections caused by Escherichia coli, Staphylococcus aureus and Klebsiella pneumoniae. Pathologia [Internet]. 2021May18 [cited 2024Mar.29];18(1):86-95. Available from: http://pat.zsmu.edu.ua/article/view/216292

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Section

Original research