Skip to main content
The American Journal of Pathology logoLink to The American Journal of Pathology
. 1987 Jul;128(1):29–44.

Response of the macaque nasal epithelium to ambient levels of ozone. A morphologic and morphometric study of the transitional and respiratory epithelium.

J R Harkema, C G Plopper, D M Hyde, J A St George, D W Wilson, D L Dungworth
PMCID: PMC1899798  PMID: 3605312

Abstract

Although ozone (O3)-induced bronchiolitis has been morphologically characterized, effects of O3 on the upper respiratory tract have not been thoroughly investigated. The purpose of this study was to determine whether exposures to ambient levels of O3 induce lesions in the nasal mucosa. Bonnet monkeys were exposed to 0.00, 0.15, or 0.30 ppm O3 for 6 or 90 days, 8 hours/day. After exposure, nasal mucosa was processed for light and electron microscopy. Quantitative changes were evident in the nasal transitional and respiratory epithelium. At 6 or 90 days of exposure to 0.15 or 0.30 ppm O3 lesions consisted of ciliated cell necrosis, shortened cilia, and secretory cell hyperplasia. Inflammatory cell influx was only present at 6 days of exposure. Ultrastructural changes in goblet cells were evident at 90 days. Ambient levels of O3 can induce significant nasal epithelial lesions, which may compromise upper respiratory defense mechanisms.

Full text

PDF
29

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Acheson E. D. Nasal cancer in the furniture and boot and shoe manufacturing industries. Prev Med. 1976 Jun;5(2):295–315. doi: 10.1016/0091-7435(76)90046-3. [DOI] [PubMed] [Google Scholar]
  2. Andersen I., Mølhave L., Proctor D. F. Human response to controlled levels of combinations of sulfur dioxide and inert dust. Scand J Work Environ Health. 1981 Mar;7(1):1–7. doi: 10.5271/sjweh.2570. [DOI] [PubMed] [Google Scholar]
  3. Boysen M., Reith A. Intracytoplasmic lumina with and without cilia in both normal and pathologically altered nasal mucosa. Ultrastruct Pathol. 1980 Oct-Dec;1(4):477–485. doi: 10.3109/01913128009140554. [DOI] [PubMed] [Google Scholar]
  4. Brain J. D. The uptake of inhaled gases by the nose. Ann Otol Rhinol Laryngol. 1970 Jun;79(3):529–539. doi: 10.1177/000348947007900315. [DOI] [PubMed] [Google Scholar]
  5. Buckley L. A., Jiang X. Z., James R. A., Morgan K. T., Barrow C. S. Respiratory tract lesions induced by sensory irritants at the RD50 concentration. Toxicol Appl Pharmacol. 1984 Jul;74(3):417–429. doi: 10.1016/0041-008x(84)90295-3. [DOI] [PubMed] [Google Scholar]
  6. Cabral-Anderson L. J., Evans M. J., Freeman G. Effects of NO2 on the lungs of rats. I. Morphology. Exp Mol Pathol. 1977 Dec;27(3):353–365. doi: 10.1016/0014-4800(77)90006-5. [DOI] [PubMed] [Google Scholar]
  7. Carson J. L., Collier A. M., Henshaw N. G., Smith C. A., Hu S. C. Response of human ciliated respiratory epithelium to brief in vivo ozone exposure: an ultrastructural study. Environ Res. 1985 Jun;37(1):212–227. doi: 10.1016/0013-9351(85)90059-3. [DOI] [PubMed] [Google Scholar]
  8. Castleman W. L., Dungworth D. L., Schwartz L. W., Tyler W. S. Acute respiratory bronchiolitis: an ultrastructural and autoradiographic study of epithelial cell injury and renewal in rhesus monkeys exposed to ozone. Am J Pathol. 1980 Mar;98(3):811–840. [PMC free article] [PubMed] [Google Scholar]
  9. Castleman W. L., Tyler W. S., Dungworth D. L. Lesions in respiratory bronchioles and conducting airways of monkeys exposed to ambient levels of ozone. Exp Mol Pathol. 1977 Jun;26(3):384–400. doi: 10.1016/0014-4800(77)90041-7. [DOI] [PubMed] [Google Scholar]
  10. Chakrin L. W., Saunders L. Z. Experimental chronic bronchitis. Pathology in the dog. Lab Invest. 1974 Feb;30(2):145–154. [PubMed] [Google Scholar]
  11. Dahl A. R., Hadley W. M., Hahn F. F., Benson J. M., McClellan R. O. Cytochrome P-450-dependent monooxygenases in olfactory epithelium of dogs: possible role in tumorigenicity. Science. 1982 Apr 2;216(4541):57–59. doi: 10.1126/science.7063870. [DOI] [PubMed] [Google Scholar]
  12. Doll R., Morgan L. G., Speizer F. E. Cancers of the lung and nasal sinuses in nickel workers. Br J Cancer. 1970 Dec;24(4):623–632. doi: 10.1038/bjc.1970.76. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eustis S. L., Schwartz L. W., Kosch P. C., Dungworth D. L. Chronic bronchiolitis in nonhuman primates after prolonged ozone exposure. Am J Pathol. 1981 Nov;105(2):121–137. [PMC free article] [PubMed] [Google Scholar]
  14. Hadley W. M., Dahl A. R. Cytochrome P-450 dependent monooxygenase activity in rat nasal epithelial membranes. Toxicol Lett. 1982 Mar;10(4):417–422. doi: 10.1016/0378-4274(82)90240-5. [DOI] [PubMed] [Google Scholar]
  15. Harris C. C., Kaufman D. G., Jackson F., Smith J. M., Dedick P., Saffiotti U. Atypical cilia in the tracheobronchial epithelium of the hamster during respiratory carcinogenesis. J Pathol. 1974 Sep;114(1):17–19. doi: 10.1002/path.1711140105. [DOI] [PubMed] [Google Scholar]
  16. Hellquist H., Irander K., Edling C., Odkvist L. M. Nasal symptoms and histopathology in a group of spray-painters. Acta Otolaryngol. 1983 Nov-Dec;96(5-6):495–500. doi: 10.3109/00016488309132736. [DOI] [PubMed] [Google Scholar]
  17. Lamb D., Reid L. Mitotic rates, goblet cell increase and histochemical changes in mucus in rat bronchial epithelium during exposure to sulphur dioxide. J Pathol Bacteriol. 1968 Jul;96(1):97–111. doi: 10.1002/path.1700960111. [DOI] [PubMed] [Google Scholar]
  18. Lippmann M. Deposition and clearance of inhaled particles in the human nose. Ann Otol Rhinol Laryngol. 1970 Jun;79(3):519–528. doi: 10.1177/000348947007900314. [DOI] [PubMed] [Google Scholar]
  19. Mellick P. W., Dungworth D. L., Schwartz L. W., Tyler W. S. Short term morphologic effects of high ambient levels of ozone on lungs of rhesus monkeys. Lab Invest. 1977 Jan;36(1):82–90. [PubMed] [Google Scholar]
  20. Miller F. J., McNeal C. A., Kirtz J. M., Gardner D. E., Coffin D. L., Menzel D. B. Nasopharyngeal removal of ozone in rabbits and guinea pigs. Toxicology. 1979 Nov;14(3):273–281. doi: 10.1016/0300-483x(79)90009-x. [DOI] [PubMed] [Google Scholar]
  21. O'Byrne P. M., Walters E. H., Aizawa H., Fabbri L. M., Holtzman M. J., Nadel J. A. Indomethacin inhibits the airway hyperresponsiveness but not the neutrophil influx induced by ozone in dogs. Am Rev Respir Dis. 1984 Aug;130(2):220–224. doi: 10.1164/arrd.1984.130.2.220. [DOI] [PubMed] [Google Scholar]
  22. O'Byrne P. M., Walters E. H., Gold B. D., Aizawa H. A., Fabbri L. M., Alpert S. E., Nadel J. A., Holtzman M. J. Neutrophil depletion inhibits airway hyperresponsiveness induced by ozone exposure. Am Rev Respir Dis. 1984 Aug;130(2):214–219. doi: 10.1164/arrd.1984.130.2.214. [DOI] [PubMed] [Google Scholar]
  23. Pedersen E., Hogetveit A. C., Andersen A. Cancer of respiratory organs among workers at a nickel refinery in Norway. Int J Cancer. 1973 Jul 15;12(1):32–41. doi: 10.1002/ijc.2910120104. [DOI] [PubMed] [Google Scholar]
  24. Plopper C. G., Morishige W. K. Alterations in granular (type II) pneumocyte ultrastructure by streptozotocin-induced diabetes in the rat. Lab Invest. 1978 Feb;38(2):143–148. [PubMed] [Google Scholar]
  25. Proctor D. F. The upper airways. I. Nasal physiology and defense of the lungs. Am Rev Respir Dis. 1977 Jan;115(1):97–129. doi: 10.1164/arrd.1977.115.1.97. [DOI] [PubMed] [Google Scholar]
  26. Snider G. L., Lucey E. C., Christensen T. G., Stone P. J., Calore J. D., Catanese A., Franzblau C. Emphysema and bronchial secretory cell metaplasia induced in hamsters by human neutrophil products. Am Rev Respir Dis. 1984 Jan;129(1):155–160. doi: 10.1164/arrd.1984.129.1.155. [DOI] [PubMed] [Google Scholar]
  27. Stephens R. J., Freeman G., Crane S. C., Furiosi N. J. Ultrastructural changes in the terminal bronchiole of the rat during continuous, low-level exposure to nitrogen dioxide. Exp Mol Pathol. 1971 Feb;14(1):1–19. doi: 10.1016/0014-4800(71)90048-7. [DOI] [PubMed] [Google Scholar]
  28. Stott W. T., McKenna M. J. The comparative absorption and excretion of chemical vapors by the upper, lower, and intact respiratory tract of rats. Fundam Appl Toxicol. 1984 Aug;4(4):594–602. doi: 10.1016/0272-0590(84)90049-6. [DOI] [PubMed] [Google Scholar]
  29. Swenberg J. A., Kerns W. D., Mitchell R. I., Gralla E. J., Pavkov K. L. Induction of squamous cell carcinomas of the rat nasal cavity by inhalation exposure to formaldehyde vapor. Cancer Res. 1980 Sep;40(9):3398–3402. [PubMed] [Google Scholar]
  30. Torjussen W., Solberg L. A., Høgetveit A. C. Histopathologic changes of nasal mucosa in nickel workers: a pilot study. Cancer. 1979 Sep;44(3):963–974. doi: 10.1002/1097-0142(197909)44:3<963::aid-cncr2820440326>3.0.co;2-h. [DOI] [PubMed] [Google Scholar]
  31. Walker D., Wilton L. V., Binns R. Inhalation toxicity studies on cigarette smoke (VII). 6-week comparative experiments using modified flue-cured cigarettes: histopathology of the conducting airways. Toxicology. 1978 Jul;10(3):241–259. doi: 10.1016/0300-483x(78)90075-6. [DOI] [PubMed] [Google Scholar]
  32. Wilhelmsson B., Lundh B. Nasal epithelium in woodworkers in the furniture industry. A histological and cytological study. Acta Otolaryngol. 1984 Sep-Oct;98(3-4):321–334. doi: 10.3109/00016488409107570. [DOI] [PubMed] [Google Scholar]
  33. Wilson D. W., Plopper C. G., Dungworth D. L. The response of the macaque tracheobronchial epithelium to acute ozone injury. A quantitative ultrastructural and autoradiographic study. Am J Pathol. 1984 Aug;116(2):193–206. [PMC free article] [PubMed] [Google Scholar]
  34. Yokoyama E., Frank R. Respiratory uptake of ozone in dogs. Arch Environ Health. 1972 Aug;25(2):132–138. doi: 10.1080/00039896.1972.10666149. [DOI] [PubMed] [Google Scholar]

Articles from The American Journal of Pathology are provided here courtesy of American Society for Investigative Pathology

RESOURCES