INTESTINAL BARRIER INTEGRITY UNDER EFFECT OF PARTICULATE MATTER FROM COTTONWOOD COMBUSTION

DOI 10.17721/1728.2748.2023.93.22-28

Authors

  • Maria Korbush Taras Shevchenko National University of Kyiv image/svg+xml
  • Ganna Tolstanova Taras Shevchenko National University of Kyiv image/svg+xml

Keywords:

particulate matter, air pollution, mucosa integrity, intestinal barrier, inflammation, colon, colitis

Abstract

The epidemiological data pointed out that exposure to ambient air pollution particulate matter (PM) may increase the risk of irritable bowel syndrome and ulcerative colitis. Air pollutants might affect the intestine through blood, mucociliary clearance of PM from the lungs, by polluted food or water intake. In the present study, we tested the hypothesis that water-suspended smoke preparations (SP) derived from the combustion of cottonwood might affect the integrity of the intestinal mucosa, induce an inflammatory response, and increase the susceptibility to chemically-induced colonic inflammation. Smoke from cottonwood was collected under laboratory conditions during the entire flaming, smouldering, and mixed combustion phases. Male Wistar rats (180-200 g) were injected with SP in two ways: 1) into the tail vein at a dose of 500 µg/100 g; 2) by gavage at a dose of 180 µg/100 g. The experimental colitis was induced 1 hour after SP injection by a single rectal injection of 0.1 ml 6% iodoacetamide (7 cm from the anus). Rats were euthanized in 2 h after colitis induction. We examined colonic vascular permeability by Evans blue extravasation (mg/g wet colon), myeloperoxidase level, total glycoprotein level at surface mucus by PAS-staining, and intestinal permeability by the translocation of bacteria into the blood of the portal vein. This study demonstrates that intravenous administration of the SP decreases the amount of surface mucus in the large intestine and increases myeloperoxidase activity in the rat colon. It did not increase the negative effect of iodoacetamide-induced colitis on changes in the state of the endothelial barrier. But, intravenous administration of SP led to the appearance of blood in the urine, which may be due to the damage to the fenestrated capillaries of the glomerulus. At the same time, oral administration of SP increased the translocation of bacteria into the blood of the portal vein which represents the increased gut permeability accompanied by a reduced level of total glycoprotein of colonic surface mucus. However, oral administration of SP did not have a significant effect on colonic vascular permeability and the activity of myeloperoxidase vs. the placebo group with colitis. The airborne PM obtained from the combustion of natural precursors such as cottonwood can cause primary pro-inflammatory changes in the intestines in a very short time after penetration into the organism through the blood and oral ingestion. Moreover, they can contribute to the violation of the integrity of the intestinal barrier.

References

Abegunde, A. T., Muhammad, B. H., Bhatti, O., & Ali, T. (2016). Environmental risk factors for inflammatory bowel diseases: Evidence based literature review. In World Journal of Gastroenterology (Vol. 22, Issue 27, pp. 6296–6317). Baishideng Publishing Group Co. https://doi.org/10.3748/wjg.v22.i27.6296

Adar, S. D., Filigrana, P. A., Clements, N., & Peel, J. L. (2014). Ambient Coarse Particulate Matter and Human Health: A Systematic Review and Meta-Analysis. Current Environmental Health Reports, 1(3), 258–274. https://doi.org/10.1007/s40572-014-0022-z

Afitska, A. I., Dovbynchuk, T. v., Holota, Y. v., Chervinska, T. M., & Tolstanova, G. M. (2015). The method of the measurement of the colonic epithelial permeability in rats during different terms of the experimental colitis. Clinical and Experimental Pathology, 14(4).

Akiba, Y., Guth, P. H., Engel, E., Nastaskin, I., Kaunitz, J. D., & Nastaskin, I. (2000). Dynamic regulation of mucus gel thickness in rat duodenum. American Journal of Physiology. Gastrointestinal and Liver Physiology, 279(2), G437–G447. https://doi.org/10.1152/ajpgi.2000.279.2.G437

Ambient (outdoor) air pollution. Accessed March 27, 2023. https://www.who.int/news-room/fact-sheets/detail/ambient-(outdoor)-air-quality-and-health

Ananthakrishnan, A. N., McGinley, E. L., Binion, D. G., & Saeian, K. (2011). Ambient air pollution correlates with hospitalizations for inflammatory bowel disease: An ecologic analysis. Inflammatory Bowel Diseases, 17(5), 1138–1145. https://doi.org/10.1002/ibd.21455

Aroui, H., Kalboussi, H., el Ghali, A., Kacem, I., Maoua, M., Maatoug, J., Taieb, D., Hamila, F., & Mrizak, N. (2018). The effect of environmental factors on the incidence of perforated appendicitis. Annali Italiani Di Chirurgia, 89, 431–437. http://europepmc.org/abstract/MED/30049910

Babadjouni, R. M., Hodis, D. M., Radwanski, R., Durazo, R., Patel, A., Liu, Q., & Mack, W. J. (2017). Clinical effects of air pollution on the central nervous system; a review. Journal of Clinical Neuroscience, 43, 16–24. https://doi.org/10.1016/j.jocn.2017.04.028

Benbrahim-Tallaa, L., Baan, R. A., Grosse, Y., Lauby-Secretan, B., el Ghissassi, F., Bouvard, V., Guha, N., Loomis, D., Straif, K., & behalf of the International Agency for Research on Cancer Monograph Working Group, on. (2012). Carcinogenicity of diesel-engine and gasoline-engine exhausts and some nitroarenes. Lancet Oncology, 13, 663–664. https://doi.org/10.1016/S1470

Borisova, T., Dekaliuk, M., Pozdnyakova, N., Pastukhov, A., Dudarenko, M., Borysov, A., Vari, S. G., & Demchenko, A. P. (2017). Harmful impact on presynaptic glutamate and GABA transport by carbon dots synthesized from sulfur-containing carbohydrate precursor. Environmental Science and Pollution Research, 24(21), 17688–17700. https://doi.org/10.1007/s11356-017-9414-6

Borisova, T., Nazarova, A., Dekaliuk, M., Krisanova, N., Pozdnyakova, N., Borysov, A., Sivko, R., & Demchenko, A. P. (2015). Neuromodulatory properties of fluorescent carbon dots: Effect on exocytotic release, uptake and ambient level of glutamate and GABA in brain nerve terminals. The International Journal of Biochemistry & Cell Biology, 59, 203–215. https://doi.org/https://doi.org/10.1016/j.biocel.2014.11.016

Borysov, A., Tarasenko, A., Krisanova, N., Pozdnyakova, N., Pastukhov, A., Dudarenko, M., Paliienko, K., & Borisova, T. (2020). Plastic smoke aerosol: Nano-sized particle distribution, absorption/fluorescent properties, dysregulation of oxidative processes and synaptic transmission in rat brain nerve terminals. Environmental Pollution, 263, 114502. https://doi.org/https://doi.org/10.1016/j.envpol.2020.114502

Brook, R. D., Franklin, B., Cascio, W., Hong, Y., Howard, G., Lipsett, M., Luepker, R., Mittleman, M., Samet, J., Smith, S. C., Jr, Tager, I., & Expert Panel on Population and Prevention Science of the American Heart Association (2004). Air pollution and cardiovascular disease: a statement for healthcare professionals from the Expert Panel on Population and Prevention Science of the American Heart Association. Circulation, 109(21), 2655–2671. https://doi.org/10.1161/01.CIR.0000128587.30041.C8

Brook, R. D., Rajagopalan, S., Pope, C. A., Brook, J. R., Bhatnagar, A., Diez-Roux, A. v., Holguin, F., Hong, Y., Luepker, R. v., Mittleman, M. A., Peters, A., Siscovick, D., Smith, S. C., Whitsel, L., & Kaufman, J. D. (2010). Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the american heart association. In Circulation (Vol. 121, Issue 21, pp. 2331–2378). https://doi.org/10.1161/CIR.0b013e3181dbece1

Burnett, R., Chen, H., Szyszkowicz, M., Fann, N., Hubbell, B., Pope, C. A., Apte, J. S., Brauer, M., Cohen, A., Weichenthal, S., Coggins, J., Di, Q., Brunekreef, B., Frostad, J., Lim, S. S., Kan, H., Walker, K. D., Thurston, G. D., Hayes, R. B., … Spadaro, J. v. (2018). Global estimates of mortality associated with long-term exposure to outdoor fine particulate matter. Proceedings of the National Academy of Sciences, 115(38), 9592–9597. https://doi.org/10.1073/pnas.1803222115

Chami, B., Martin, N. J. J., Dennis, J. M., & Witting, P. K. (2018). Myeloperoxidase in the inflamed colon: A novel target for treating inflammatory bowel disease. In Archives of Biochemistry and Biophysics (Vol. 645, pp. 61–71). Academic Press Inc. https://doi.org/10.1016/j.abb.2018.03.012

Costa, L. G., Cole, T. B., Dao, K., Chang, Y.-C., Coburn, J., & Garrick, J. M. (2020). Effects of air pollution on the nervous system and its possible role in neurodevelopmental and neurodegenerative disorders. Pharmacology & Therapeutics, 210, 107523. https://doi.org/https://doi.org/10.1016/j.pharmthera.2020.107523

De Brouwere, K., Buekers, J., Cornelis, C., Schlekat, C. E., & Oller, A. R. (2012). Assessment of indirect human exposure to environmental sources of nickel: oral exposure and risk characterization for systemic effects. The Science of the total environment, 419, 25–36. https://doi.org/10.1016/j.scitotenv.2011.12.049

Derrien, M., van Passel, M. W. J., van de Bovenkamp, J. H. B., Schipper, R. G., de Vos, W. M., & Dekker, J. (2010). Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes, 1(4), 254–268. https://doi.org/10.4161/gmic.1.4.12778

Dorofeyev, A., Dorofeyeva, A., Borysov, A., Tolstanova, G., & Borisova, T. (2022). Gastrointestinal health: changes of intestinal mucosa and microbiota in patients with ulcerative colitis and irritable bowel syndrome from PM2.5-polluted regions of Ukraine. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-022-22710-9

Duan, R., Wu, Y., Wang, M., Wu, J., Wang, X., Wang, Z., Hu, Y., & Duan, L. (2021). Association between short-term exposure to fine particulate pollution and outpatient visits for ulcerative colitis in Beijing, China: A time–series study. Ecotoxicology and Environmental Safety, 214, 112116. https://doi.org/https://doi.org/10.1016/j.ecoenv.2021.112116

Duerr, R. H., Taylor, K. D., Brant, S. R., Rioux, J. D., Silverberg, M. S., Daly, M. J., Steinhart, A. H., Abraham, C., Regueiro, M., Griffiths, A., Dassopoulos, T., Bitton, A., Yang, H., Targan, S., Datta, L. W., Kistner, E. O., Schumm, L. P., Lee, A. T., Gregersen, P. K., … Cho, J. H. (2006). A Genome-Wide Association Study Identifies IL23R as an Inflammatory Bowel Disease Gene. Science, 314(5804), 1461–1463. https://doi.org/10.1126/science.1135245

Holota, Y. v., Olefir, Y. A., Dovbynchuk, T. v., & Tolstanova, G. M. (2016). Carbohydrate composition of rat intestine surface mucus layer after ceftriaxone treatment. Ukrainian Biochemical Journal, 88(6), 35–44. https://doi.org/10.15407/ubj88.06.035

Kaplan, G. G., Dixon, E., Panaccione, R., Fong, A., Chen, L., Szyszkowicz, M., Wheeler, A., MacLean, A., Buie, W. D., Leung, T., Heitman, S. J., & Villeneuve, P. J. (2009). Effect of ambient air pollution on the incidence of appendicitis. Canadian Medical Association Journal, 181(9), 591. https://doi.org/10.1503/cmaj.082068

Kilian, J., & Kitazawa, M. (2018). The emerging risk of exposure to air pollution on cognitive decline and Alzheimer’s disease – Evidence from epidemiological and animal studies. Biomedical Journal, 41(3), 141–162. https://doi.org/https://doi.org/10.1016/j.bj.2018.06.001

Kish, L., Hotte, N., Kaplan, G. G., Vincent, R., Tso, R., Gänzle, M., Rioux, K. P., Thiesen, A., Barkema, H. W., Wine, E., & Madsen, K. L. (2013). Environmental Particulate Matter Induces Murine Intestinal Inflammatory Responses and Alters the Gut Microbiome. PLOS ONE, 8(4), e62220-. https://doi.org/10.1371/journal.pone.0062220

Kronman, M. P., Zaoutis, T. E., Haynes, K., Feng, R., & Coffin, S. E. (2012). Antibiotic Exposure and IBD Development Among Children: A Population-Based Cohort Study. Pediatrics, 130(4), e794–e803. https://doi.org/10.1542/peds.2011-3886

Kucharzik, T., Koletzko, S., Kannengießer, K., & Dignaß, A. (2020). Colitis ulcerosa - Diagnostische und therapeutische Algorithmen. Deutsches Arzteblatt International, 117(33–34), 564–573. https://doi.org/10.3238/arztebl.2020.0564

Landrigan, P. J., Fuller, R., Acosta, N. J. R., Adeyi, O., Arnold, R., Basu, N. (Nil), Baldé, A. B., Bertollini, R., Bose-O’Reilly, S., Boufford, J. I., Breysse, P. N., Chiles, T., Mahidol, C., Coll-Seck, A. M., Cropper, M. L., Fobil, J., Fuster, V., Greenstone, M., Haines, A., … Zhong, M. (2018). The Lancet Commission on pollution and health. In The Lancet (Vol. 391, Issue 10119, pp. 462–512). Lancet Publishing Group. https://doi.org/10.1016/S0140-6736(17)32345-0

Larauche, M., Gourcerol, G., Wang, L., Pambukchian, K., Brunnhuber, S., Adelson, D. W., Rivier, J., Million, M., & Taché, Y. (2009). Cortagine, a CRF 1 agonist, induces stresslike alterations of colonic function and visceral hypersensitivity in rodents primarily through peripheral pathways. Am J Physiol Gastrointest Liver Physiol, 297, 215–227. https://doi.org/10.1152/ajpgi.00072.2009.-Corticotropin

Lewis, T. C., Robins, T. G., Dvonch, J. T., Keeler, G. J., Yip, F. Y., Mentz, G. B., Lin, X., Parker, E. A., Israel, B. A., Gonzalez, L., & Hill, Y. (2005). Air pollution-associated changes in lung function among asthmatic children in Detroit. Environmental Health Perspectives, 113(8), 1068–1075. https://doi.org/10.1289/ehp.7533

Loomis, D., Grosse, Y., Lauby-Secretan, B., Ghissassi, F. el, Bouvard, V., Benbrahim-Tallaa, L., Guha, N., Baan, R., Mattock, H., & Straif, K. (2013). The carcinogenicity of outdoor air pollution. The Lancet Oncology, 14(13), 1262–1263. https://doi.org/10.1016/S1470-2045(13)70487-X

López-Abente, G., García-Pérez, J., Fernández-Navarro, P., Boldo, E., & Ramis, R. (2012). Colorectal cancer mortality and industrial pollution in Spain. BMC Public Health, 12(1), 589. https://doi.org/10.1186/1471-2458-12-589

M’koma, A. E. (2013). Inflammatory Bowel Disease: An Expanding Global Health Problem. Clinical Medicine Insights: Gastroenterology, 6, CGast.S12731. https://doi.org/10.4137/CGast.S12731

Mak, W. Y., Zhao, M., Ng, S. C., & Burisch, J. (2020). The epidemiology of inflammatory bowel disease: East meets west. In Journal of Gastroenterology and Hepatology (Australia) (Vol. 35, Issue 3, pp. 380–389). Blackwell Publishing. https://doi.org/10.1111/jgh.14872

Möller, W., Häussinger, K., Ziegler-Heitbrock, L., & Heyder, J. (2006). Mucociliary and long-term particle clearance in airways of patients with immotile cilia. Respiratory research, 7(1), 10. https://doi.org/10.1186/1465-9921-7-10

Mutlu, E. A., Engen, P. A., Soberanes, S., Urich, D., Forsyth, C. B., Nigdelioglu, R., Chiarella, S. E., Radigan, K. A., Gonzalez, A., Jakate, S., Keshavarzian, A., Budinger, G. R. S., & Mutlu, G. M. (2011). Particulate matter air pollution causes oxidant-mediated increase in gut permeability in mice. Particle and Fibre Toxicology, 8(1), 19. https://doi.org/10.1186/1743-8977-8-19

Nemmar, A., Hoet, P. H., Vanquickenborne, B., Dinsdale, D., Thomeer, M., Hoylaerts, M. F., Vanbilloen, H., Mortelmans, L., & Nemery, B. (2002). Passage of inhaled particles into the blood circulation in humans. Circulation, 105(4), 411–414. https://doi.org/10.1161/hc0402.104118

Orsini Delgado, M. L., Sambuelli, A., Negreira, S., Gil, A., D′Elia, L., Smaldini, P. L., & Docena, G. H. (2022). Volcanic ash-driven worsening of mucosal inflammation in an experimental colitis model. Environmental Pollution, 292, 118351. https://doi.org/https://doi.org/10.1016/j.envpol.2021.118351

Paliienko K, Korbush M, Krisanova N, et al. Similar in vitro response of rat brain nerve terminals, colon preparations and COLO 205 cells to smoke particulate matter from different types of wood. Neurotoxicology. 2022;93:244-256.

Percie du Sert, N., Ahluwalia, A., Alam, S., Avey, M. T., Baker, M., Browne, W. J., Clark, A., Cuthill, I. C., Dirnagl, U., Emerson, M., Garner, P., Holgate, S. T., Howells, D. W., Hurst, V., Karp, N. A., Lazic, S. E., Lidster, K., MacCallum, C. J., Macleod, M., … Würbel, H. (2020). Reporting animal research: Explanation and elaboration for the ARRIVE guidelines 2.0. PLOS Biology, 18(7), e3000411-. https://doi.org/10.1371/journal.pbio.3000411

Pöschl U. (2005). Atmospheric aerosols: composition, transformation, climate and health effects. Angewandte Chemie (International ed. in English), 44(46), 7520–7540. https://doi.org/10.1002/anie.200501122

Pražnikar,Z. & Pražnikar,J.(2012).The effects of particulate matter air pollution on respiratory health and on the cardiovascular system. Slovenian Journal of Public Health,51(3) 190-199. https://doi.org/10.2478/v10152-012-0022-z

Saiki, T. (1998). Myeloperoxidase Concentrations in the Stool as a New Parameter of Inflammatory Bowel Disease. In Kurume Medical Journal (Vol. 45).

Salim, S. Y., Jovel, J., Wine, E., Kaplan, G. G., Vincent, R., Thiesen, A., Barkema, H. W., & Madsen, K. L. (2014). Exposure to Ingested Airborne Pollutant Particulate Matter Increases Mucosal Exposure to Bacteria and Induces Early Onset of Inflammation in Neonatal IL-10–Deficient Mice. Inflammatory Bowel Diseases, 20(7), 1129–1138. https://doi.org/10.1097/MIB.0000000000000066

Satoh, H., Sato, F., Takami, K., & Szabo, S. (1997). New Ulcerative Colitis Model Induced by Sulfhydryl Blockers in Rats and the Effects of Antiinflammatory Drugs on the Colitis. The Japanese Journal of Pharmacology, 73(4), 299–309. https://doi.org/10.1254/jjp.73.299

Scientific Committee on Food. (2002). Opinion of the Scientific Committee on Food on the risks to human health of Polycyclic Aromatic Hydrocarbons in food. http://europa.eu.int/comm/food/fs/sc/scf/index_en.htm

Shelestov, A., Kolotii, A., Borisova, T., Turos, O., Milinevsky, G., Gomilko, I., Bulanay, T., Fedorov, O., Shumilo, L., Pidgorodetska, L., Kolos, L., Borysov, A., Pozdnyakova, N., Chunikhin, A., Dudarenko, M., Petrosian, A., Danylevsky, V., Miatselskaya, N., & Choliy, V. (2020). Essential variables for air quality estimation. International Journal of Digital Earth, 13(2), 278–298. https://doi.org/10.1080/17538947.2019.1620881

Soon, I. S., Molodecky, N. A., Rabi, D. M., Ghali, W. A., Barkema, H. W., & Kaplan, G. G. (2012). The relationship between urban environment and the inflammatory bowel diseases: a systematic review and meta-analysis. BMC Gastroenterology, 12(1), 51. https://doi.org/10.1186/1471-230X-12-51

Stetska, V. O., Dovbynchuk, T. v, Makedon, Y. S., & Dziubenko, N. v. (2021). The effect of water-soluble pristine C60 fullerene on 6-OHDA-induced Parkinson’s disease in rats. Regulatory Mechanisms in Biosystems, 12(4). https://doi.org/10.15421/022182

Strous, G. J., Dekker, J., & Hiii, R. L. (1992). Mucin-Type Glycoproteins Referee. In Critical Reviews in Biochemistry and Molecular Biology (Vol. 27, Issue 2).

Tarasenko, A., Pozdnyakova, N., Paliienko, K., Borysov, A., Krisanova, N., Pastukhov, A., Stanovyi, O., Gnatyuk, O., Dovbeshko, G., & Borisova, T. (2022). A comparative study of wood sawdust and plastic smoke particulate matter with a focus on spectroscopic, fluorescent, oxidative, and neuroactive properties. Environmental Science and Pollution Research, 29(25), 38315–38330. https://doi.org/10.1007/s11356-022-18741-x

Veauthier, B., & Hornecker, J. R. (2018). Crohn’s Disease: Diagnosis and Management. American Family Physician, 98(11), 661–669.

World Health Assembly, 68. (‎2015)‎. Health and the environment: addressing the health impact of air pollution. World Health Organization. https://apps.who.int/iris/handle/10665/253237

Published

2025-10-17