Advertisement

International Ophthalmology

, Volume 39, Issue 10, pp 2283–2294 | Cite as

Mechanism of interaction between ocular and nasal neurogenic inflammation in allergic rhinoconjunctivitis

  • Xiao-Wei Gao
  • Xiao-Min ZhangEmail author
  • Hai-Yan Liu
  • Shan-Shan Wang
  • Hua-Jiang Dong
Original Paper
  • 57 Downloads

Abstract

Purpose

The mechanisms of naso-ocular interaction in allergic rhinoconjunctivitis are not well understood. Neurogenic inflammation affects both eyes and nose via the same neurogenic factors. The purpose of this study was to investigate the effects of neurogenic inflammation on conjunctival inflammation following nasal allergen provocation.

Methods

Sensitized rats were exposed to ovalbumin (OVA) via the nose. Parts of the nasal mucosa and conjunctivae were sliced and used for hematoxylin–eosin staining, immunohistochemical analysis, western blotting, and real-time polymerase chain reaction. The slides were observed under a light microscope, and the acquired images were analyzed. The levels of substance P (SP), vasoactive intestinal peptide (VIP), and nerve growth factor (NGF) were detected.

Results

The levels of SP, VIP, and NGF were increased in both nasal mucosa and conjunctivae 1 h and 24 h after OVA administration (p < 0.05). Higher levels of SP, VIP, and NGF expression were observed in the nasal mucosa and conjunctivae 24 h after OVA administration (p < 0.05). Following damage of the nasal sensory nerves by capsaicin, the protein and mRNA levels of SP, VIP, and NGF were reduced.

Conclusion

In conclusion, the increased levels of VIP, SP, and NGF might be responsible for the ocular reaction following nasal challenge with allergen in rats.

Keywords

Allergic rhinoconjunctivitis Conjunctiva Nerve growth factor Substance P Vasoactive intestinal peptide 

Notes

Acknowledgements

We thank Dr. Hong Zhang for her expert assistance. We would also like to thank teacher Yue Ming Wang for his advice and help with the animal experiment. This study was supported by animal laboratory of Institute of Biomedical Engineering, Chinese Academy of Medical Sciences and Peking Union Medical College, Tianjin, China.

Funding

No funding was required for this study.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interests.

Ethical approval

All procedures were approved by the Institutional Animal Care and Use Committee of Tianjin Medical University and conducted in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals.

Human and animal rights

All the ethical standards for animal handling and experimentation were followed in this study.

References

  1. 1.
    Johansson SG, Bieber T, Dahl R et al (2004) Revised nomenclature for allergy for global use: report of the Nomenclature Review Committee of the World Allergy Organization, October 2003. J Allergy Clin Immunol 113:832–836.  https://doi.org/10.1016/j.jaci.2003.12.591 CrossRefPubMedGoogle Scholar
  2. 2.
    Blaiss MS (2007) Allergic rhinoconjunctivitis: burden of disease. Allergy Asthma Proc 28:393–397.  https://doi.org/10.2500/aap.2007.28.3013 CrossRefPubMedGoogle Scholar
  3. 3.
    Pallasaho P, Juusela M, Lindqvist A et al (2011) Allergic rhinoconjunctivitis doubles the risk for incident asthma—results from a population study in Helsinki, Finland. Respir Med 105:1449–1456.  https://doi.org/10.1016/j.rmed.2011.04.013 CrossRefPubMedGoogle Scholar
  4. 4.
    O’Meara TJ, Sercombe JK, Morgan G et al (2005) The reduction of rhinitis symptoms by nasal filters during natural exposure to ragweed and grass pollen. Allergy 60:529–532.  https://doi.org/10.1111/j.1398-9995.2005.00741.x CrossRefPubMedGoogle Scholar
  5. 5.
    Baroody FM, Foster KA, Markaryan A et al (2008) Nasal ocular reflexes and eye symptoms in patients with allergic rhinitis. Ann Allergy Asthma Immunol 100:194–199.  https://doi.org/10.1016/S1081-1206(10)60442-5 CrossRefPubMedGoogle Scholar
  6. 6.
    Baroody FM, Shenaq D, DeTineo M et al (2009) Fluticasone furoate nasal spray reduces the nasal-ocular reflex: a mechanism for the efficacy of topical steroids in controlling allergic eye symptoms. J Allergy Clin Immunol 123:1342–1348.  https://doi.org/10.1016/j.jaci.2009.03.015 CrossRefPubMedGoogle Scholar
  7. 7.
    Callebaut I, Spielberg L, Hox V et al (2010) Conjunctival effects of a selective nasal pollen provocation. Allergy 65:1173–1181.  https://doi.org/10.1111/j.1398-9995.2010.02360.x CrossRefPubMedGoogle Scholar
  8. 8.
    Lightman S, Scadding GK (2012) Should intranasal corticosteroids be used for the treatment of ocular symptoms of allergic rhinoconjunctivitis? A review of their efficacy and safety profile. Int Arch Allergy Immunol 158:317–325.  https://doi.org/10.1159/000333100 CrossRefPubMedGoogle Scholar
  9. 9.
    Baroody FM, Logothetis H, Vishwanath S et al (2013) Effect of intranasal fluticasone furoate and intraocular olopatadine on nasal and ocular allergen-induced symptoms. Am J Rhinol Allergy 27:48–53.  https://doi.org/10.2500/ajra.2013.27.3841 CrossRefPubMedGoogle Scholar
  10. 10.
    Richardson JD, Vasko MR (2002) Cellular mechanisms of neurogenic inflammation. J Pharmacol Exp Ther 302:839–845.  https://doi.org/10.1124/jpet.102.032797 CrossRefPubMedGoogle Scholar
  11. 11.
    Pelikan Z (2010) Allergic conjunctivitis and nasal allergy. Curr Allergy Asthma Rep 10:295–302.  https://doi.org/10.1007/s11882-010-0119-x CrossRefPubMedGoogle Scholar
  12. 12.
    Naclerio RM, Pinto J, deTineo M et al (2008) Elucidating the mechanism underlying the ocular symptoms associated with allergic rhinitis. Allergy Asthma Proc 29:24–28.  https://doi.org/10.2500/aap2008.29.3075 CrossRefPubMedGoogle Scholar
  13. 13.
    Undem BJ, Kajekar R, Hunter DD et al (2000) Neural integration and allergic disease. J Allergy Clin Immunol 106:S213–S220CrossRefGoogle Scholar
  14. 14.
    Meredith SD, Raphael GD, Baraniuk JN et al (1989) The pathophysiology of rhinitis. III. The control of IgG secretion. J Allergy Clin Immunol 84:920–930CrossRefGoogle Scholar
  15. 15.
    Micera A, Lambiase A, Bonini S (2008) The role of neuromediators in ocular allergy. Curr Opin Allergy Clin Immunol 8:466–471.  https://doi.org/10.1097/ACI.0b013e32830e6b17 CrossRefPubMedGoogle Scholar
  16. 16.
    Daoud A, Xie Z, Ma Y et al (2014) Changes of T-helper type 1/2 cell balance by anticholinergic treatment in allergic mice. Ann Allergy Asthma Immunol 112:249–255.  https://doi.org/10.1016/j.anai.2013.12.014 CrossRefPubMedGoogle Scholar
  17. 17.
    Li T, Zhao C (2015) A preliminary study on the role of substance P in histamine-nasal-spray-induced allergic conjunctivitis in guinea pigs. Zhonghua Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 50:836–841PubMedGoogle Scholar
  18. 18.
    Bresciani M, Lalibertè F, Lalibertè MF et al (2009) Nerve growth factor localization in the nasal mucosa of patients with persistent allergic rhinitis. Allergy 64:112–117.  https://doi.org/10.1111/j.1398-9995.2008.01831.x CrossRefPubMedGoogle Scholar
  19. 19.
    Motterle L, Diebold Y, Enríquez de Salamanca A et al (2006) Altered expression of neurotransmitter receptors and neuromediators in vernal keratoconjunctivitis. Arch Ophthalmol 124:462–468.  https://doi.org/10.1001/archopht.124.4.462 CrossRefPubMedGoogle Scholar
  20. 20.
    Callebaut I, De Vries A, Steelant B et al (2014) Nasal allergen deposition leads to conjunctival mast cell degranulation in allergic rhinoconjunctivitis. Am J Rhinol Allergy 28:290–296.  https://doi.org/10.2500/ajra.2014.28.4052 CrossRefPubMedGoogle Scholar
  21. 21.
    Callebaut I, Vandewalle E, Hox V et al (2012) Nasal corticosteroid treatment reduces substance P levels in tear fluid in allergic rhinoconjunctivitis. Ann Allergy Asthma Immunol 109:141–146.  https://doi.org/10.1016/j.anai.2012.06.008 CrossRefPubMedGoogle Scholar
  22. 22.
    Soslow RA, Dannenberg AJ, Rush D et al (2000) COX-2 is expressed in human pulmonary, colonic, and mammary tumors. Cancer 89:2637–2645CrossRefGoogle Scholar
  23. 23.
    Hicke-Roberts A, Åberg N, Wennergren G et al (2017) Allergic rhinoconjunctivitis continued to increase in Swedish children up to 2007, but asthma and eczema levelled off from 1991. Acta Paediatr 106:75–80.  https://doi.org/10.1111/apa.13433 CrossRefPubMedGoogle Scholar
  24. 24.
    Anthracopoulos MB, Fouzas S, Pandiora A et al (2011) Prevalence trends of rhinoconjunctivitis, eczema, and atopic asthma in Greek schoolchildren: four surveys during 1991–2008. Allergy Asthma Proc 32:56–62.  https://doi.org/10.2500/aap.2011.32.3504 CrossRefPubMedGoogle Scholar
  25. 25.
    Baroody FM, Naclerio RM (2011) Nasal-ocular reflexes and their role in the management of allergic rhinoconjunctivitis with intranasal steroids. World Allergy Org 4:S1–S5.  https://doi.org/10.1097/WOX.0b013e3181f32dcd CrossRefGoogle Scholar
  26. 26.
    Celander O, Folkow B (1953) The nature and the distribution of afferent fibres provided with the axon reflex arrangement. Acta Physiol Scand 29:359–370.  https://doi.org/10.1111/j.1748-1716.1953.tb01032.x CrossRefPubMedGoogle Scholar
  27. 27.
    Naclerio R (2008) Intranasal corticosteroids reduce ocular symptoms associated with allergic rhinitis. Otolaryngol Head Neck Surg 138:129–139.  https://doi.org/10.1016/j.otohns.2007.10.027 CrossRefPubMedGoogle Scholar
  28. 28.
    Van Gerven L, Alpizar YA, Wouters MM et al (2014) Capsaicin treatment reduces nasal hyperreactivity and transient receptor potential cation channel subfamily V, receptor 1 (TRPV1) overexpression in patients with idiopathic rhinitis. J Allergy Clin Immunol 133(1332–9):1339.e1–1339.e3.  https://doi.org/10.1016/j.jaci.2013.08.026 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Tianjin Medical University Eye Institute and Tianjin Medical University School of Optometry and OphthalmologyTianjin Medical University Eye HospitalTianjinChina
  2. 2.Department of Otolaryngology-Head and Neck SurgerySecond Hospital of Tianjin Medical UniversityTianjinChina
  3. 3.State Key Laboratory of Precision Measurement Technology and InstrumentsTianjin UniversityTianjinChina

Personalised recommendations