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Seasonal variation in submacular hemorrhages in retinal macroaneurysms and its disappearance in age-related macular degeneration

  • Retinal Disorders
  • Published:
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Abstract

Purpose

To investigate whether previously reported seasonal variation and winter-dominant prevalence of acute massive submacular hemorrhages (SMHs) caused by age-related macular degeneration (AMD) disappeared, and those caused by retinal microaneurysms (RMAs) emerged.

Method

The medical charts of 95 patients (95 eyes) with SMH caused by AMD and 76 patients (76 eyes) with SMH caused by RMAs in 2012–2019 were retrospectively reviewed. For each subject, the month of onset, the mean ambient temperature of that month were recorded.

Results

The monthly numbers of cases of SMHs caused by AMD from January to December were 6, 8, 4, 9, 7, 10, 9, 11, 7, 11, 3, and 10. No significant seasonal variation in the monthly incidence was identified (Roger’s R = 1.89, p = 0.39). The monthly numbers of SMHs caused by RMAs from January to December were 3, 11, 11, 8, 7, 8, 5, 5, 2, 4, 7, and 5. There was significant seasonal variation in the monthly incidence (Roger’s R = 7.67, p = 0.02). There was no significant correlation between the monthly incidence of SMHs caused by RMAs and mean ambient temperature.

Conclusion

Our previous study conducted for cases obtained in 1998–2005 showed seasonal cyclic trend in the number of SMHs caused by AMD, with the peak in winter. However, that significant seasonal variation disappeared in 2012–2019 in the present study. Common usage of OCT devices and anti-VEGF drugs might be the reason for the lack of seasonal variation in the cases of SMH caused by AMD.

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Data availability

All data and material are available from supplementary material.

Code availability

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References

  1. Berrocal MH, Lewis ML, Flynn HW Jr (1996) Variations in the clinical course of submacular hemorrhage. Am J Ophthalmol 122:486–493

    Article  CAS  Google Scholar 

  2. Humayun M, Lewis H, Flynn HW Jr, Sternberg P Jr, Blumenkranz MS (1998) Management of submacular hemorrhage associated with retinal arterial macroaneurysms. Am J Ophthalmol 126:358–361

    Article  CAS  Google Scholar 

  3. Ibanez HE, Williams DF, Thomas MA, Ruby AJ, Meredith TA, Boniuk I, Grand MG (1995) Surgical management of submacular hemorrhage: a series of 47 consecutive cases. Arch Ophthalmol-Chic 113:62–69

    Article  CAS  Google Scholar 

  4. Stanescu-Segall D, Balta F, Jackson TL (2016) Submacular hemorrhage in neovascular age-related macular degeneration: a synthesis of the literature. Surv Ophthalmol 61:18–32

    Article  Google Scholar 

  5. Panton RW, Goldberg MF, Farber MD (1990) Retinal arterial macroaneurysms: risk factors and natural history. Br J Ophthalmol 74:595–600

    Article  CAS  Google Scholar 

  6. Chakravarthy U, Wong TY, Fletcher A, Piault E, Evans C, Zlateva G, Buggage R, Pleil A, Mitchell P (2010) Clinical risk factors for age-related macular degeneration: a systematic review and meta-analysis. BMC Ophthalmol 10:31

    Article  Google Scholar 

  7. Robertson D (1973) Macroaneurysm of the retinal arteries. Trans Am Acad Ophthalmol 77:55–67

    Google Scholar 

  8. Rabb MF, Gagliano DA, Teske MP (1988) Retinal arterial macroaneurysms. Surv Ophthalmol 33:73–96

    Article  CAS  Google Scholar 

  9. Haberman S, Capildeo R, Rose FC (1981) The seasonal variation in mortality from cerebrovascular disease. J Neurol Sci 52:25–36

    Article  CAS  Google Scholar 

  10. Shinkawa A, Ueda K, Hasuo Y, Kiyohara Y, Fujishima M (1990) Seasonal variation in stroke incidence in Hisayama, Japan. Stroke; a journal of cerebral circulation 21:1262–1267

    Article  CAS  Google Scholar 

  11. Iguchi Y, Ito Y, Kikuchi M, Ishikawa K, Oshima H, Yatsuya H, Terasaki H (2006) Seasonal variations of acute massive submacular haemorrhage associated with age-related macular degeneration. Br J Ophthalmol 90:1256–1258

    Article  CAS  Google Scholar 

  12. Nam JM (1996) Detection of cyclic trends in incidence data using the efficiency score method. Biom J 38:661–668

    Article  Google Scholar 

  13. Castillo MM, Mowatt G, Elders A, Lois N, Fraser C, Hernández R, Amoaku W, Burr JM, Lotery A, Ramsay CR, Azuara-Blanco A (2015) Optical coherence tomography for the monitoring of neovascular age-related macular degeneration: a systematic review. Ophthalmology 122:399–406

    Article  Google Scholar 

  14. Kim KH, Kim JH, Chang YS, Lee TG, Kim JW, Lew YJ (2015) Clinical outcomes of eyes with submacular hemorrhage secondary to age-related macular degeneration treated with anti-vascular endothelial growth factor. Korean J Ophthalmol 29:315–324

    Article  CAS  Google Scholar 

  15. Cruickshanks KJ, Klein R, Klein BE, Nondahl DM (2001) Sunlight and the 5-year incidence of early age-related maculopathy: the beaver dam eye study. Arch Ophthalmol 119:246–50

    CAS  PubMed  Google Scholar 

  16. Tomany SC, Cruickshanks KJ, Klein R, Klein BE, Knudtson MD (2004) Sunlight and the 10-year incidence of age-related maculopathy: the Beaver Dam Eye Study. Arch Ophthalmol 122:750–7

    Article  Google Scholar 

  17. Brockmann C, Brockmann T, Dawczynski J (2013) Influence of seasonal sunlight intensity and iris color on the anti-VEGF therapy for neovascular age-related macular degeneration. Eye (Lond) 27:1169–1173

    Article  CAS  Google Scholar 

  18. Brennan P, Greenberg G, Miall W, Thompson S (1982) Seasonal variation in arterial blood pressure. Br Med J (Clin Res Ed) 285:919–923

    Article  CAS  Google Scholar 

  19. Hozawa A, Kuriyama S, Shimazu T, Ohmori-Matsuda K, Tsuji I (2011) Seasonal variation in home blood pressure measurements and relation to outside temperature in Japan. Clin Exp Hypertens 33:153–158

    Article  Google Scholar 

  20. Fukuda H, Ninomiya H, Ueba Y, Ohta T, Kaneko T, Kadota T, Hamada F, Fukui N, Nonaka M, Watari Y, Nishimoto S, Fukuda M, Hayashi S, Izumidani T, Nishimura H, Moriki A, Lo B, Ueba T (2020) Impact of temperature decline from the previous day as a trigger of spontaneous subarachnoid hemorrhage: case-crossover study of prefectural stroke database. J Neurosurg 133:374–382

    Article  Google Scholar 

  21. Smith RA, Edwards PR, Da Silva AF (2008) Are periods of low atmospheric pressure associated with an increased risk of abdominal aortic aneurysm rupture? Ann R Coll Surg Engl 90:389–393

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank Ms. Kumi Fujiwara, Mr. Keigo Omori, and Ms. Waka Miyagi for technical assistance. We thank Claire Barnes, PhD, from Edanz Group (https://en-author-services.edanz.com/ac) for editing a draft of this manuscript.

Funding

This work was partially supported by Grants-in-Aid for Scientific Research (C) (H.K., 19K09988) from JSPS KAKENHI (http://www.jsps.go.jp/), the Eye Research Foundation for the Aged (ERFA, H.K.), Charitable Trust Fund for Ophthalmic Research in Commemoration of Santen Pharmaceutical’s Founder (H.K.), Bayer Retina Award Foundation (H.K.), Ichihara International Scholarship Foundation (H.K.), and Aichi Health Promotion Foundation (H.K.).

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Authors and Affiliations

  1. Department of Ophthalmology, Nagoya University Graduate School of Medicine, Nagoya, Japan

    Hiroki Kaneko, Noriko Takashi, Yasuki Ito, Jun Takeuchi, Hiroko Terasaki & Koji M. Nishiguchi

  2. Department of Public Health, Fujita Health University School of Medicine, Aichi, Japan

    Masaaki Matsunaga & Hiroshi Yatsuya

  3. Department of Ophthalmology, Fujita Health University School of Medicine, Aichi, Japan

    Yasuki Ito

  4. Institutes of Innovation for Future Society, Nagoya University, Nagoya, Japan

    Hiroko Terasaki

  5. Department of Public Health and Health Systems, Nagoya University Graduate School of Medicine, Nagoya, Japan

    Hiroshi Yatsuya

Authors
  1. Hiroki Kaneko
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  2. Noriko Takashi
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  3. Masaaki Matsunaga
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  4. Yasuki Ito
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  5. Jun Takeuchi
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  6. Hiroko Terasaki
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  7. Hiroshi Yatsuya
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  8. Koji M. Nishiguchi
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Contributions

Acquisition of data: H.K., N.T., Y.I.

Analysis and interpretation of data: H.K., M.M.

Drafting of manuscript: H.K., M.M., H.Y.

Critical revision: J.T., H.T., H.Y., K.M.N.

Corresponding author

Correspondence to Hiroki Kaneko.

Ethics declarations

Ethics approval and consent to participate

The procedures adhered to the tenets of the World Medical Association’s Declaration of Helsinki. The Nagoya University Hospital ethics review board approved this retrospective analysis of patient records. The review board waived the requirement for informed consent because of the retrospective nature of the study.

Consent for publication

All authors have approved the manuscript and agree with submission to Graefe’s Archive for Clinical and Experimental Ophthalmology.

Conflict of interest

The authors declare no competing interests.

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The funding institutions that supported this study had no role in the design or conduct of this research.

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Kaneko, H., Takashi, N., Matsunaga, M. et al. Seasonal variation in submacular hemorrhages in retinal macroaneurysms and its disappearance in age-related macular degeneration . Graefes Arch Clin Exp Ophthalmol 259, 3589–3596 (2021). https://doi.org/10.1007/s00417-021-05280-3

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  • DOI: https://doi.org/10.1007/s00417-021-05280-3

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