Morphological and Functional Changes of Meibomian Glands in Pediatric and Adult Patients with Allergic Conjunctivitis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Subjects
2.2. Clinical Evaluation
2.3. Multi-Parametric Automated Meibomian Gland Analyzer
2.4. Statistical Analysis
3. Results
3.1. Characteristics and Clinical Indexes
3.2. Comparison of the Meibomian Gland Morphological and Functional Changes Observed in the Pediatric Group and the Adult Group
3.3. Factors Related to the Percentage Change in GA
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Leonardi, A.; Castegnaro, A.; Valerio, A.L.; Lazzarini, D. Epidemiology of allergic conjunctivitis: Clinical appearance and treatment patterns in a population-based study. Curr. Opin. Allergy Clin. Immunol. 2015, 15, 482–488. [Google Scholar] [CrossRef] [PubMed]
- Feng, Y.; Wang, X.; Wang, F.; Liu, R.; Chen, L.; Wu, S.; Yang, X.; Chen, M.; Rao, Y.; Li, J. The Prevalence of Ocular Allergy and Comorbidities in Chinese School Children in Shanghai. Biomed. Res. Int. 2017, 2017, 7190987. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fauquert, J. Diagnosing and managing allergic conjunctivitis in childhood: The allergist’s perspective. Pediatr. Allergy Immunol. 2019, 30, 405–414. [Google Scholar] [CrossRef] [PubMed]
- Gomes, P. Trends in prevalence and treatment of ocular allergy. Curr. Opin. Allergy Clin. Immunol. 2014, 14, 451–456. [Google Scholar] [CrossRef] [PubMed]
- Chen, M.; Wei, A.; Ke, B.; Zou, J.; Gong, L.; Wang, Y.; Zhang, C.; Xu, J.; Yin, J.; Hong, J. Combination of 0.05% Azelastine and 0.1% Tacrolimus Eye Drops in Children With Vernal Keratoconjunctivitis: A Prospective Study. Front. Med. 2021, 8, 650083. [Google Scholar] [CrossRef]
- Vazirani, J.; Shukla, S.; Chhawchharia, R.; Sahu, S.; Gokhale, N.; Basu, S. Allergic conjunctivitis in children: Current understanding and future perspectives. Curr. Opin. Allergy Clin. Immunol. 2020, 20, 507–515. [Google Scholar] [CrossRef]
- Solomon, A. Corneal complications of vernal keratoconjunctivitis. Curr. Opin. Allergy Clin. Immunol. 2015, 15, 489–494. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Li, J.; Liu, R.; Lao, H.; Fan, Z.; Jin, L.; Liang, L.; Liu, Y. Association of Allergic Conjunctivitis With Health-Related Quality of Life in Children and Their Parents. JAMA Ophthalmol. 2021, 139, 830–837. [Google Scholar] [CrossRef] [PubMed]
- Pawankar, R. Allergic diseases and asthma: A global public health concern and a call to action. World Allergy Organ. J. 2014, 7, 12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Strube, Y. Drawing Attention to the Burden of Allergic Conjunctivitis in Children and Their Families. JAMA Ophthalmol. 2021, 139, 837–838. [Google Scholar] [CrossRef] [PubMed]
- Villani, E.; Rabbiolo, G.; Nucci, P. Ocular allergy as a risk factor for dry eye in adults and children. Curr. Opin. Allergy Clin. Immunol. 2018, 18, 398–403. [Google Scholar] [CrossRef] [PubMed]
- Stapleton, F.; Alves, M.; Bunya, V.Y.; Jalbert, I.; Lekhanont, K.; Malet, F.; Na, K.-S.; Schaumberg, D.; Uchino, M.; Vehof, J.; et al. TFOS DEWS II Epidemiology Report. Ocul. Surf. 2017, 15, 334–365. [Google Scholar] [CrossRef] [PubMed]
- Akil, H.; Celik, F.; Ulas, F.; Kara, I. Dry Eye Syndrome and Allergic Conjunctivitis in the Pediatric Population. Middle E. Afr. J Ophthalmol. 2015, 22, 467–471. [Google Scholar] [CrossRef] [Green Version]
- Chen, L.; Pi, L.; Fang, J.; Chen, X.; Ke, N.; Liu, Q. High incidence of dry eye in young children with allergic conjunctivitis in Southwest China. Acta Ophthalmol. 2016, 94, e727–e730. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bron, A.; de Paiva, C.; Chauhan, S.; Bonini, S.; Gabison, E.; Jain, S.; Knop, E.; Markoulli, M.; Ogawa, Y.; Perez, V.; et al. TFOS DEWS II pathophysiology report. Ocul. Surf. 2017, 15, 438–510. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.; Applebaum, D.; Sun, G.; Pflugfelder, S. Atopic keratoconjunctivitis: A review. J. Am. Acad. Dermatol. 2014, 70, 569–575. [Google Scholar] [CrossRef] [PubMed]
- Guglielmetti, S.; Dart, J.; Calder, V. Atopic keratoconjunctivitis and atopic dermatitis. Curr. Opin. Allergy Clin. Immunol. 2010, 10, 478–485. [Google Scholar] [CrossRef]
- Ibrahim, O.M.; Matsumoto, Y.; Dogru, M.; Adan, E.S.; Wakamatsu, T.H.; Shimazaki, J.; Fujishima, H.; Tsubota, K. In vivo confocal microscopy evaluation of meibomian gland dysfunction in atopic-keratoconjunctivitis patients. Ophthalmology 2012, 119, 1961–1968. [Google Scholar] [CrossRef] [PubMed]
- Arita, R.; Itoh, K.; Maeda, S.; Maeda, K.; Tomidokoro, A.; Amano, S. Association of contact lens-related allergic conjunctivitis with changes in the morphology of meibomian glands. Jpn. J. Ophthalmol. 2012, 56, 14–19. [Google Scholar] [CrossRef]
- Arita, R.I.K.; Maeda, S.; Maeda, K.; Furuta, A.; Tomidokoro, A.; Amano, S. Meibomian gland duct distortion in patients with perennial allergic conjunctivitis. Cornea 2010, 29, 850–860. [Google Scholar] [CrossRef]
- Mizoguchi, S.; Iwanishi, H.; Arita, R.; Shirai, K.; Sumioka, T.; Kokado, M.; Jester, J.V.; Saika, S. Ocular surface inflammation impairs structure and function of meibomian gland. Exp. Eye Res. 2017, 163, 78–84. [Google Scholar] [CrossRef]
- Reyes, N.; Yu, C.; Mathew, R.; Kunnen, C.; Kalnitsky, J.; Redfern, R.; Leonardi, A.; Perez, V.; MacLeod, A.; Gupta, P.; et al. Neutrophils cause obstruction of eyelid sebaceous glands in inflammatory eye disease in mice. Sci. Transl. Med. 2018, 10, eaas9164. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mahajan, A.; Hasikova, L.; Hampel, U.; Gruneboom, A.; Shan, X.; Herrmann, I.; Garreis, F.; Bock, F.; Knopf, J.; Singh, J.; et al. Aggregated neutrophil extracellular traps occlude Meibomian glands during ocular surface inflammation. Ocul. Surf. 2021, 20, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Arita, R.; Suehiro, J.; Haraguchi, T.; Maeda, S.; Maeda, K.; Tokoro, H.; Amano, S. Topical diquafosol for patients with obstructive meibomian gland dysfunction. Br. J. Ophthalmol. 2013, 97, 725–729. [Google Scholar] [CrossRef] [PubMed]
- Aronowicz, J.; Shine, W.; Oral, D.; Vargas, J.; McCulley, J. Short term oral minocycline treatment of meibomianitis. Br. J. Ophthalmol. 2006, 90, 856–860. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Finis, D.; König, C.; Hayajneh, J.; Borrelli, M.; Schrader, S.; Geerling, G. Six-month effects of a thermodynamic treatment for MGD and implications of meibomian gland atrophy. Cornea 2014, 33, 1265–1270. [Google Scholar] [CrossRef] [PubMed]
- Yin, Y.; Gong, L. Reversibility of Gland Dropout and Significance of Eyelid Hygiene Treatment in Meibomian Gland Dysfunction. Cornea 2017, 36, 332–337. [Google Scholar] [CrossRef] [PubMed]
- Yin, Y.; Liu, N.; Gong, L.; Song, N. Changes in the Meibomian Gland After Exposure to Intense Pulsed Light in Meibomian Gland Dysfunction (MGD) Patients. Curr. Eye Res. 2018, 43, 308–313. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hura, A.S.; Epitropoulos, A.T.; Czyz, C.N.; Rosenberg, E.D. Visible Meibomian Gland Structure Increases After Vectored Thermal Pulsation Treatment in Dry Eye Disease Patients with Meibomian Gland Dysfunction. Clin. Ophthalmol. 2020, 14, 4287–4296. [Google Scholar] [CrossRef]
- Yang, B.; Wen, K.; Li, J.; Zhang, S.; Fan, Z.; Liang, X.; Liang, L. Quantitative evaluation of lipid layer thickness and blinking in children with allergic conjunctivitis. Graefe’s Arch. Clin. Exp. Ophthalmol. 2021, 259, 2795–2805. [Google Scholar] [CrossRef]
- Wolffsohn, J.S.A.R.; Chalmers, R.; Djalilian, A.; Dogru, M.; Dumbleton, K.; Gupta, P.K.; Karpecki, P.; Lazreg, S.; Pult, H.; Sullivan, B.D.; et al. TFOS DEWS II Diagnostic Methodology report. Ocul. Surf. 2017, 15, 539–574. [Google Scholar] [CrossRef] [PubMed]
- Arita, R.I.K.; Inoue, K.; Amano, S. Noncontact infrared meibography to document age-related changes of the meibomian glands in a normal population. Ophthalmology 2008, 115, 911–915. [Google Scholar] [CrossRef] [PubMed]
- Deng, Y.; Wang, Q.; Luo, Z.; Li, S.; Wang, B.; Zhong, J.; Peng, L.; Xiao, P.; Yuan, J. Quantitative analysis of morphological and functional features in Meibography for Meibomian Gland Dysfunction: Diagnosis and Grading. EClinicalMedicine 2021, 40. [Google Scholar] [CrossRef] [PubMed]
- Xiao, P.; Luo, Z.; Deng, Y.; Wang, G.; Yuan, J. An automated and multiparametric algorithm for objective analysis of meibography images. Quant. Imaging Med. Surg. 2021, 11, 1586–1599. [Google Scholar] [CrossRef] [PubMed]
- Le, Q.; Hong, J.; Zhu, W.; Sun, X.; Xu, J. In vivo laser scanning confocal microscopy of vernal keratoconjunctivitis. Clin. Exp. Ophthalmol. 2011, 39, 53–60. [Google Scholar] [CrossRef]
- Wei, Q.; Le, Q.; Hong, J.; Xiang, J.; Wei, A.; Xu, J. In vivo confocal microscopy of meibomian glands and palpebral conjunctiva in vernal keratoconjunctivitis. Indian J. Ophthalmol. 2015, 63, 327–330. [Google Scholar] [CrossRef]
- Villani, E.M.L.; Dellavalle, A.; Serafino, M.; Nucci, P. Latest evidences on meibomian gland dysfunction diagnosis and management. Ocul. Surf. 2020, 18, 871–892. [Google Scholar] [CrossRef] [PubMed]
- Koh, Y.; Celik, T.; Lee, H.; Petznick, A.; Tong, L. Detection of meibomian glands and classification of meibography images. J. Biomed. Opt. 2012, 17, 086008. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tomlinson, A.; Bron, A.; Korb, D.; Amano, S.; Paugh, J.; Pearce, E.; Yee, R.; Yokoi, N.; Arita, R.; Dogru, M. The international workshop on meibomian gland dysfunction: Report of the diagnosis subcommittee. Investig. Ophthalmol. Vis. Sci. 2011, 52, 2006–2049. [Google Scholar] [CrossRef] [PubMed]
- Ban, Y.; Shimazaki-Den, S.; Tsubota, K.; Shimazaki, J. Morphological Evaluation of Meibomian Glands Using Noncontact Infrared Meibography. Ocul. Surf. 2013, 11, 47–53. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wu, Y.; Li, H.; Tang, Y.; Yan, X. Morphological Evaluation of Meibomian Glands in Children and Adolescents Using Noncontact Infrared Meibography. J. Pediatr. Ophthalmol. Strabismus 2017, 54, 78–83. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Parfitt, G.; Xie, Y.; Geyfman, M.; Brown, D.; Jester, J. Absence of ductal hyper-keratinization in mouse age-related meibomian gland dysfunction (ARMGD). Aging 2013, 5, 825–834. [Google Scholar] [CrossRef] [Green Version]
- Sullivan, D.A.; Rocha, E.M.; Aragona, P.; Clayton, J.A.; Ding, J.; Golebiowski, B.; Hampel, U.; McDermott, A.M.; Schaumberg, D.A.; Srinivasan, S.; et al. TFOS DEWS II Sex, Gender, and Hormones Report. Ocul. Surf. 2017, 15, 284–333. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.; Chen, S.; Wang, S.; Chen, Y.; Li, J.; Fu, Y.; Dai, Q.; Lin, X.; Wu, Y.; Zhao, Y. The significance of meibomian gland changes in asymptomatic children. Ocul. Surf. 2018, 16, 301–305. [Google Scholar] [CrossRef] [PubMed]
- Daniel, E.M.M.; Pistilli, M.; Bunya, V.Y.; Massaro-Giordano, G.M.; Smith, E.; Kadakia, P.A.; Asbell, P.A.; Dry Eye Assessment and Management (DREAM) Study Research Group. Grading and baseline characteristics of meibomian glands in meibography images and their clinical associations in the Dry Eye Assessment and Management (DREAM) study. Ocul. Surf. 2019, 17, 491–501. [Google Scholar] [CrossRef]
- McDonnell, J.; Weller, K.; Pien, L.C. Safety of Intranasal Steroids: An Updated Perspective. Curr. Allergy Asthma Rep. 2020, 20, 69. [Google Scholar] [CrossRef]
Variables | Children (N = 30) | Range (Min, Max) | Adults (N = 29) | Range (Min, Max) | p |
---|---|---|---|---|---|
Age, year | 7.83 ± 2.67 | (4, 15) | 39.59 ± 12.37 | (17, 60) | <0.001 |
Sex, n (%) | <0.001 | ||||
Male | 27 (90.0) | 11 (37.9) | |||
Female | 3 (10.0) | 18 (62.1) | |||
Onset duration, month | 4.6 ± 4.2 | (2.0, 24.0) | 3.9 ± 4.1 | (0.3, 24.0) | 0.176 |
Treatment duration, day | 34.77 ± 14.12 | (21, 75) | 49.79 ± 28.11 | (13, 119) | <0.05 |
Treatment therapy, n (%) | <0.001 | ||||
Regimen 1 a | 0 (0.0) | 10 (34.5) | |||
Regimen 2 b | 0 (0.0) | 11 (37.9) | |||
Regimen 3 c | 30 (100.0) | 8 (27.6) | |||
CFS (0–3) | 0.10 ± 0.40 | (0, 2) | 0.17 ± 0.47 | (0, 2) | 0.386 |
Upper MGL (0–3) | 0.77 ± 0.68 | (0, 3) | 1.07 ± 0.65 | (0, 3) | 0.052 |
NIBUT-1st, s | 4.67 ± 3.05 | (1.08, 14.65) | 5.73 ± 3.06 | (1.21, 14.31) | 0.091 |
NIBUT-avg, s | 5.88 ± 3.56 | (1.08, 14.65) | 6.86 ± 2.90 | (1.21, 14.31) | 0.110 |
TMH, mm | 0.18 ± 0.03 | (0.14, 0.25) | 0.20 ± 0.03 | (0.15, 0.23) | 0.103 |
Group | Total | The Percentage Change in GA (%) a, n (%) | p | ||||||
---|---|---|---|---|---|---|---|---|---|
Decrease | NC | Improve | |||||||
>10 | 5–10 | <5 | 0 | <5 | 5–10 | >10 | |||
Pediatric | 30 | 3.3 | 3.3 | 3.3 | 3.3 | 23.3 | 30.0 | 33.3 | 0.001 |
Adult | 29 | 24.1 | 6.9 | 13.8 | 17.2 | 27.6 | 3.4 | 6.9 |
Characteristic at Baseline | Age | Sex a | Onset Duration | Treatment Duration | Upper MGL | GA | TI | SI |
---|---|---|---|---|---|---|---|---|
r | −0.54 | −0.49 | 0.06 | −0.194 | 0.02 | −0.35 | −0.51 | −0.38 |
p | <0.001 | <0.001 | 0.656 | 0.149 | 0.870 | 0.009 | <0.001 | 0.004 |
Difference value of other indexes | ΔTI b | ΔSI | ΔNIBUT-1st | ΔNIBUT-avg | ||||
r | 0.19 | 0.15 | 0.05 | 0.14 | ||||
p | 0.150 | 0.261 | 0.720 | 0.287 |
Predictor | Unstandardized Coefficients Beta | Standardized Coefficients Beta | 95% CI | p | |
---|---|---|---|---|---|
Lower | Upper | ||||
Age | −0.28 | −0.44 | −0.45 | −0.12 | 0.001 |
Sexa | −3.55 | −0.15 | −9.42 | 2.32 | 0.230 |
TI | −0.37 | −0.15 | −0.92 | 0.19 | 0.189 |
GA | −0.55 | −0.42 | −0.82 | −0.29 | <0.001 |
SI | 0.24 | 0.04 | −1.46 | 1.94 | 0.780 |
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Wu, Y.; Jiang, H.; Zhou, X.; Zhai, Z.; Yang, P.; Zhou, S.; Gu, H.; Xu, J.; Hong, J. Morphological and Functional Changes of Meibomian Glands in Pediatric and Adult Patients with Allergic Conjunctivitis. J. Clin. Med. 2022, 11, 1427. https://doi.org/10.3390/jcm11051427
Wu Y, Jiang H, Zhou X, Zhai Z, Yang P, Zhou S, Gu H, Xu J, Hong J. Morphological and Functional Changes of Meibomian Glands in Pediatric and Adult Patients with Allergic Conjunctivitis. Journal of Clinical Medicine. 2022; 11(5):1427. https://doi.org/10.3390/jcm11051427
Chicago/Turabian StyleWu, Yuqing, Hao Jiang, Xujiao Zhou, Zimeng Zhai, Pei Yang, Shuyun Zhou, Hao Gu, Jianjiang Xu, and Jiaxu Hong. 2022. "Morphological and Functional Changes of Meibomian Glands in Pediatric and Adult Patients with Allergic Conjunctivitis" Journal of Clinical Medicine 11, no. 5: 1427. https://doi.org/10.3390/jcm11051427
APA StyleWu, Y., Jiang, H., Zhou, X., Zhai, Z., Yang, P., Zhou, S., Gu, H., Xu, J., & Hong, J. (2022). Morphological and Functional Changes of Meibomian Glands in Pediatric and Adult Patients with Allergic Conjunctivitis. Journal of Clinical Medicine, 11(5), 1427. https://doi.org/10.3390/jcm11051427