The status in the mechanism and significance of the hyperreflective foci in macular edema by optical coherence tomography_Chinese Journal of Ocular Fundus Diseases

Authors：

Xiao Shiyu ,  Yang Liu

Department of Ophthalmology, Peking University First Hospital, Beijing 100034, China;

Corresponding author：

Yang Liu, Email: liu_yang@bjmu.edu.cn

Keywords：

Macular edema; Tomography, optical coherence; Review; Hyperreflective foci

DOI：

10.3760/cma.j.cn511434-20200417-00168

Video：

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Abstract Full text Figures/Tables Video References Cited by

Macular edema is an important cause of visual impairment in many eye diseases such as diabetic retinopathy, retinal vein occlusion and uveitis. Optical coherence tomography (OCT) provides high-resolution image of retinal microstructures in a non-contact and rapid manner, which greatly improves the ability of diagnosis and follow-up to macular edema patients. OCT has been widely used in the clinical detection of patients with macular edema. No matter what the cause of macular edema is, it can be observed in OCT images that there are spot-like deposits with strong reflection signals in the retina, which are mostly distributed discretely or partially convergent, and are called hyperreflective foci. At present, the nature or source of hyperreflective foci is not clear, however, may involve the destruction of the blood retina barrier, retinal inflammatory reaction, neurocellular degeneration, and so on. These mechanisms are also the key physiological mechanisms in the development of macular edema. The clinical research on hyperreflective foci provides a new direction for understanding the pathogenesis of macular edema and predicting the prognosis of macular edema. The distribution and quantity characteristics of hyperreflective foci may be an important biological marker to predict the prognosis of macular edema.nosis of macular edema. foci provides a new direction for understanding the pathogenesis of macular edema and predicting the prognosis of macular edema. The distribution and quantity characteristics of HRF may be an important biological marker to predict the prognosis of macular edema.

Citation： Xiao Shiyu, Yang Liu. The status in the mechanism and significance of the hyperreflective foci in macular edema by optical coherence tomography. Chinese Journal of Ocular Fundus Diseases, 2021, 37(7): 572-576. doi: 10.3760/cma.j.cn511434-20200417-00168 Copy

1.	Coscas G, Cunha-Vaz J, Soubrane G. Macular edema: definition and basic concepts[J]. Dev Ophthalmol, 2010, 47: 1-9. DOI: 10.1159/000320070.
2.	Framme C, Schweizer P, Imesch M, et al. Behavior of SD-OCT-detected hyperreflective foci in the retina of anti-VEGF-treated patients with diabetic macular edema[J]. Invest Ophthalmol Vis Sci, 2012, 53(9): 5814-5818. DOI: 10.1167/iovs.12-9950.
3.	Bolz M, Schmidt-Erfurth U, Deak G, et al. Optical coherence tomographic hyperreflective foci: a morphologic sign of lipid extravasation in diabetic macular edema[J]. Ophthalmology, 2009, 116(5): 914-920. DOI: 10.1016/j.ophtha.2008.12.039.
4.	Coscas G, De Benedetto U, Coscas F, et al. Hyperreflective dots: a new spectral-domain optical coherence tomography entity for follow-up and prognosis in exudative age-related macular degeneration[J]. Ophthalmologica, 2013, 229(1): 32-37. DOI: 10.1159/000342159.
5.	Uji A, Murakami T, Nishijima K, et al. Association between hyperreflective foci in the outer retina, status of photoreceptor layer, and visual acuity in diabetic macular edema[J]. Am J Ophthalmol, 2012, 153(4): 710-717. DOI: 10.1016/j.ajo.2011.08.041.
6.	Ogino K, Murakami T, Tsujikawa A, et al. Characteristics of optical coherence tomographic hyperreflective foci in retinal vein occlusion[J]. Retina, 2012, 32(1): 77-85. DOI: 10.1097/IAE.0b013e318217ffc7.
7.	Coscas G, Gaudric A. Natural course of nonaphakic cystoid macular edema[J]. Surv Ophthalmol, 1984, 28(Suppl): S471-484. DOI: 10.1016/0039-6257(84)90229-7.
8.	Deák GG, Bolz M, Ritter M, et al. A systematic correlation between morphology and functional alterations in diabetic macular edema[J]. Invest Ophthalmol Vis Sci, 2010, 51(12): 6710-6714. DOI: 10.1167/iovs.09-5064.
9.	Ota M, Nishijima K, Sakamoto A, et al. Optical coherence tomographic evaluation of foveal hard exudates in patients with diabetic maculopathy accompanying macular detachment[J]. Ophthalmology, 2010, 117(10): 1996-2002. DOI: 10.1016/j.ophtha.2010.06.019.
10.	Niu S, Yu C, Chen Q, et al. Multimodality analysis of hyper-reflective foci and hard exudates in patients with diabetic retinopathy[J/OL]. Sci Rep, 2017, 7(1): 1568[2017-05-08]. https://pubmed.ncbi.nlm.nih.gov/28484225/. DOI: 10.1038/s41598-017-01733-0.
11.	刘广峰, 蔺洁, 范颖, 等. 非增生型糖尿病视网膜病变黄斑水肿患者黄斑区谱域光学相干断层扫描中高反射信号的特征分析[J]. 眼科新进展, 2013, 33(4): 331-334.Liu, GF, Lin J, Fan Y, et al. Characteristics of hyperreflective foci in SD-OCT of macular area in patients with DME of non-proliferative diabetic retinopathy[J]. Rec Adv Ophthalmol, 2013, 33(4): 331-334.
12.	Klaassen I, Van Noorden CJ, Schlingemann RO. Molecular basis of the inner blood-retinal barrier and its breakdown in diabetic macular edema and other pathological conditions[J]. Prog Retin Eye Res, 2013, 34: 19-48. DOI: 10.1016/j.preteyeres.2013.02.001.
13.	Sorrentino FS, Allkabes M, Salsini G, et al. The importance of glial cells in the homeostasis of the retinal microenvironment and their pivotal role in the course of diabetic retinopathy[J]. Life Sci, 2016, 162: 54-59. DOI: 10.1016/j.lfs.2016.08.001.
14.	Colonna M, Butovsky O. Microglia function in the central nervous system during health and neurodegeneration[J]. Annu Rev Immunol, 2017, 35: 441-468. DOI: 10.1146/annurev-immunol-051116-052358.
15.	McMenamin PG, Saban DR, Dando SJ. Immune cells in the retina and choroid: two different tissue environments that require different defenses and surveillance[J]. Prog Retin Eye Res, 2019, 70: 85-98. DOI: 10.1016/j.preteyeres.2018.12.002.
16.	Huang T, Cui J, Li L, et al. The role of microglia in the neurogenesis of zebrafish retina[J]. Biochem Biophys Res Commun, 2012, 421(2): 214-220. DOI: 10.1016/j.bbrc.2012.03.139.
17.	Cardona SM, Mendiola AS, Yang YC, et al. Disruption of fractalkine signaling leads to microglial activation and neuronal damage in the diabetic retina[J/OL]. ASN Neuro, 2015, 7(5): 1759091415608204[2015-10-29]. https://pubmed.ncbi.nlm.nih.gov/26514658/. DOI: 10.1177/1759091415608204.
18.	Tang Y, Le W. Differential roles of M1 and M2 microglia in neurodegenerative diseases[J]. Mol Neurobiol, 2016, 53(2): 1181-1194. DOI: 10.1007/s12035-014-9070-5.
19.	Bogdanov P, Corraliza L, Villena JA, et al. The db/db mouse: a useful model for the study of diabetic retinal neurodegeneration[J/OL]. PLoS One, 2014, 9(5): e97302[2014-05-16]. https://pubmed.ncbi.nlm.nih.gov/24837086/. DOI: 10.1371/journal.pone.0097302.
20.	Xu H, Chen M, Forrester JV. Para-inflammation in the aging retina[J]. Prog Retin Eye Res, 2009, 28(5): 348-368. DOI: 10.1016/j.preteyeres.2009.06.001.
21.	Vujosevic S, Bini S, Midena G, et al. Hyperreflective intraretinal spots in diabetics without and with nonproliferative diabetic retinopathy: an in vivo study using spectral domain OCT[J/OL]. J Diabetes Res, 2013, 2013: 491835[2013-12-09]. https://pubmed.ncbi.nlm.nih.gov/24386645/. DOI: 10.1155/2013/491835.
22.	Schreur V, Altay L, van Asten F, et al. Hyperreflective foci on optical coherence tomography associate with treatment outcome for anti-VEGF in patients with diabetic macular edema[J/OL]. PLoS One, 2018, 13(10): e0206482[2018-08-31]. https://pubmed.ncbi.nlm.nih.gov/30379920/. DOI: 10.1371/journal.pone.0206482.
23.	Li M, Dolz-Marco R, Messinger JD, et al. Clinicopathologic correlation of anti-vascular endothelial growth factor-treated type 3 neovascularization in age-related macular degeneration[J]. Ophthalmology, 2018, 125(2): 276-287. DOI: 10.1016/j.ophtha.2017.08.019.
24.	Berasategui B, Fonollosa A, Artaraz J, et al. Behavior of hyperreflective foci in non-infectious uveitic macular edema, a 12-month follow-up prospective study[J/OL]. BMC Ophthalmol, 2018, 18(1): 179[2018-07-20]. https://pubmed.ncbi.nlm.nih.gov/30029623/. DOI: 10.1186/s12886-018-0848-5.
25.	Lee H, Jang H, Choi YA, et al. Association between soluble CD14 in the aqueous humor and hyperreflective foci on optical coherence tomography in patients with diabetic macular edema[J]. Invest Ophthalmol Vis Sci, 2018, 59(2): 715-721. DOI: 10.1167/iovs.17-23042.
26.	Landmann R, Müller B, Zimmerli W. CD14, new aspects of ligand and signal diversity[J]. Microbes Infect, 2000, 2(3): 295-304. DOI: 10.1016/s1286-4579(00)00298-7.
27.	Yin GN, Jeon H, Lee S, et al. Role of soluble CD14 in cerebrospinal fluid as a regulator of glial functions[J]. J Neurosci Res, 2009, 87(11): 2578-2590. DOI: 10.1002/jnr.22081.
28.	Ascaso FJ, Huerva V, Grzybowski A. The role of inflammation in the pathogenesis of macular edema secondary to retinal vascular diseases[J/OL]. Mediators Inflamm, 2014, 2014: 432685[2014-07-22]. https://pubmed.ncbi.nlm.nih.gov/25152567/. DOI: 10.1155/2014/432685.
29.	Daruich A, Matet A, Moulin A, et al. Mechanisms of macular edema: beyond the surface[J]. Prog Retin Eye Res, 2018, 63: 20-68. DOI: 10.1016/j.preteyeres.2017.10.006.
30.	Marmor MF. Mechanisms of fluid accumulation in retinal edema[J]. Doc Ophthalmol, 1999, 97(3-4): 239-249. DOI: 10.1023/a: 1002192829817.
31.	Bunt-Milam AH, Saari JC, Klock IB, et al. Zonulae adherentes pore size in the external limiting membrane of the rabbit retina[J]. Invest Ophthalmol Vis Sci, 1985, 26(10): 1377-1380.
32.	Gardner TW, Antonetti DA, Barber AJ, et al. Diabetic retinopathy: more than meets the eye[J]. Surv Ophthalmol, 2002, 47(Suppl 2): S253-262. DOI: 10.1016/s0039-6257(02)00387-9.
33.	Tso MO, Cunha-Vaz JG, Shih CY, et al. Clinicopathologic study of blood-retinal barrier in experimental diabetes mellitus[J]. Arch Ophthalmol, 1980, 98(11): 2032-2040. DOI: 10.1001/archopht.1980.01020040884020.
34.	Cunha-Vaz J, Ashton P, Iezzi R, et al. Sustained delivery fluocinolone acetonide vitreous implants: long-term benefit in patients with chronic diabetic macular edema[J]. Ophthalmology, 2014, 121(10): 1892-1903. DOI: 10.1016/j.ophtha.2014.04.019.
35.	Kang JW, Lee H, Chung H, et al. Correlation between optical coherence tomographic hyperreflective foci and visual outcomes after intravitreal bevacizumab for macular edema in branch retinal vein occlusion[J]. Graefe's Arch Clin Exp Ophthalmol, 2014, 252(9): 1413-1421. DOI: 10.1007/s00417-014-2595-5.
36.	Chatziralli IP, Sergentanis TN, Sivaprasad S. Hyperreflective foci as an independent visual outcome predictor in macular edema due to retinal vascular diseases treated with intravitreal dexamethasone or ranibizumab[J]. Retina, 2016, 36(12): 2319-2328. DOI: 10.1097/IAE.0000000000001070.
37.	Kang JW, Chung H, Chan Kim H. Correlation of optical coherence tomographic hyperreflective foci with visual outcomes in different patterns of diabetic macular edema[J]. Retina, 2016, 36(9): 1630-1639. DOI: 10.1097/IAE.0000000000000995.
38.	Hwang HS, Chae JB, Kim JY, et al. Association between hyperreflective dots on spectral-domain optical coherence tomography in macular edema and response to treatment[J]. Invest Ophthalmol Vis Sci, 2017, 58(13): 5958-5967. DOI: 10.1167/iovs.17-22725.
39.	Liu S, Wang D, Chen F, et al. Hyperreflective foci in OCT image as a biomarker of poor prognosis in diabetic macular edema patients treating with conbercept in China[J/OL]. BMC Ophthalmol, 2019, 19(1): 157[2019-07-23]. https://pubmed.ncbi.nlm.nih.gov/31337360/. DOI: 10.1186/s12886-019-1168-0.

1. Coscas G, Cunha-Vaz J, Soubrane G. Macular edema: definition and basic concepts[J]. Dev Ophthalmol, 2010, 47: 1-9. DOI: 10.1159/000320070.
2. Framme C, Schweizer P, Imesch M, et al. Behavior of SD-OCT-detected hyperreflective foci in the retina of anti-VEGF-treated patients with diabetic macular edema[J]. Invest Ophthalmol Vis Sci, 2012, 53(9): 5814-5818. DOI: 10.1167/iovs.12-9950.
3. Bolz M, Schmidt-Erfurth U, Deak G, et al. Optical coherence tomographic hyperreflective foci: a morphologic sign of lipid extravasation in diabetic macular edema[J]. Ophthalmology, 2009, 116(5): 914-920. DOI: 10.1016/j.ophtha.2008.12.039.
4. Coscas G, De Benedetto U, Coscas F, et al. Hyperreflective dots: a new spectral-domain optical coherence tomography entity for follow-up and prognosis in exudative age-related macular degeneration[J]. Ophthalmologica, 2013, 229(1): 32-37. DOI: 10.1159/000342159.
5. Uji A, Murakami T, Nishijima K, et al. Association between hyperreflective foci in the outer retina, status of photoreceptor layer, and visual acuity in diabetic macular edema[J]. Am J Ophthalmol, 2012, 153(4): 710-717. DOI: 10.1016/j.ajo.2011.08.041.
6. Ogino K, Murakami T, Tsujikawa A, et al. Characteristics of optical coherence tomographic hyperreflective foci in retinal vein occlusion[J]. Retina, 2012, 32(1): 77-85. DOI: 10.1097/IAE.0b013e318217ffc7.
7. Coscas G, Gaudric A. Natural course of nonaphakic cystoid macular edema[J]. Surv Ophthalmol, 1984, 28(Suppl): S471-484. DOI: 10.1016/0039-6257(84)90229-7.
8. Deák GG, Bolz M, Ritter M, et al. A systematic correlation between morphology and functional alterations in diabetic macular edema[J]. Invest Ophthalmol Vis Sci, 2010, 51(12): 6710-6714. DOI: 10.1167/iovs.09-5064.
9. Ota M, Nishijima K, Sakamoto A, et al. Optical coherence tomographic evaluation of foveal hard exudates in patients with diabetic maculopathy accompanying macular detachment[J]. Ophthalmology, 2010, 117(10): 1996-2002. DOI: 10.1016/j.ophtha.2010.06.019.
10. Niu S, Yu C, Chen Q, et al. Multimodality analysis of hyper-reflective foci and hard exudates in patients with diabetic retinopathy[J/OL]. Sci Rep, 2017, 7(1): 1568[2017-05-08]. https://pubmed.ncbi.nlm.nih.gov/28484225/. DOI: 10.1038/s41598-017-01733-0.
11. 刘广峰, 蔺洁, 范颖, 等. 非增生型糖尿病视网膜病变黄斑水肿患者黄斑区谱域光学相干断层扫描中高反射信号的特征分析[J]. 眼科新进展, 2013, 33(4): 331-334.Liu, GF, Lin J, Fan Y, et al. Characteristics of hyperreflective foci in SD-OCT of macular area in patients with DME of non-proliferative diabetic retinopathy[J]. Rec Adv Ophthalmol, 2013, 33(4): 331-334.
12. Klaassen I, Van Noorden CJ, Schlingemann RO. Molecular basis of the inner blood-retinal barrier and its breakdown in diabetic macular edema and other pathological conditions[J]. Prog Retin Eye Res, 2013, 34: 19-48. DOI: 10.1016/j.preteyeres.2013.02.001.
13. Sorrentino FS, Allkabes M, Salsini G, et al. The importance of glial cells in the homeostasis of the retinal microenvironment and their pivotal role in the course of diabetic retinopathy[J]. Life Sci, 2016, 162: 54-59. DOI: 10.1016/j.lfs.2016.08.001.
14. Colonna M, Butovsky O. Microglia function in the central nervous system during health and neurodegeneration[J]. Annu Rev Immunol, 2017, 35: 441-468. DOI: 10.1146/annurev-immunol-051116-052358.
15. McMenamin PG, Saban DR, Dando SJ. Immune cells in the retina and choroid: two different tissue environments that require different defenses and surveillance[J]. Prog Retin Eye Res, 2019, 70: 85-98. DOI: 10.1016/j.preteyeres.2018.12.002.
16. Huang T, Cui J, Li L, et al. The role of microglia in the neurogenesis of zebrafish retina[J]. Biochem Biophys Res Commun, 2012, 421(2): 214-220. DOI: 10.1016/j.bbrc.2012.03.139.
17. Cardona SM, Mendiola AS, Yang YC, et al. Disruption of fractalkine signaling leads to microglial activation and neuronal damage in the diabetic retina[J/OL]. ASN Neuro, 2015, 7(5): 1759091415608204[2015-10-29]. https://pubmed.ncbi.nlm.nih.gov/26514658/. DOI: 10.1177/1759091415608204.
18. Tang Y, Le W. Differential roles of M1 and M2 microglia in neurodegenerative diseases[J]. Mol Neurobiol, 2016, 53(2): 1181-1194. DOI: 10.1007/s12035-014-9070-5.
19. Bogdanov P, Corraliza L, Villena JA, et al. The db/db mouse: a useful model for the study of diabetic retinal neurodegeneration[J/OL]. PLoS One, 2014, 9(5): e97302[2014-05-16]. https://pubmed.ncbi.nlm.nih.gov/24837086/. DOI: 10.1371/journal.pone.0097302.
20. Xu H, Chen M, Forrester JV. Para-inflammation in the aging retina[J]. Prog Retin Eye Res, 2009, 28(5): 348-368. DOI: 10.1016/j.preteyeres.2009.06.001.
21. Vujosevic S, Bini S, Midena G, et al. Hyperreflective intraretinal spots in diabetics without and with nonproliferative diabetic retinopathy: an in vivo study using spectral domain OCT[J/OL]. J Diabetes Res, 2013, 2013: 491835[2013-12-09]. https://pubmed.ncbi.nlm.nih.gov/24386645/. DOI: 10.1155/2013/491835.
22. Schreur V, Altay L, van Asten F, et al. Hyperreflective foci on optical coherence tomography associate with treatment outcome for anti-VEGF in patients with diabetic macular edema[J/OL]. PLoS One, 2018, 13(10): e0206482[2018-08-31]. https://pubmed.ncbi.nlm.nih.gov/30379920/. DOI: 10.1371/journal.pone.0206482.
23. Li M, Dolz-Marco R, Messinger JD, et al. Clinicopathologic correlation of anti-vascular endothelial growth factor-treated type 3 neovascularization in age-related macular degeneration[J]. Ophthalmology, 2018, 125(2): 276-287. DOI: 10.1016/j.ophtha.2017.08.019.
24. Berasategui B, Fonollosa A, Artaraz J, et al. Behavior of hyperreflective foci in non-infectious uveitic macular edema, a 12-month follow-up prospective study[J/OL]. BMC Ophthalmol, 2018, 18(1): 179[2018-07-20]. https://pubmed.ncbi.nlm.nih.gov/30029623/. DOI: 10.1186/s12886-018-0848-5.
25. Lee H, Jang H, Choi YA, et al. Association between soluble CD14 in the aqueous humor and hyperreflective foci on optical coherence tomography in patients with diabetic macular edema[J]. Invest Ophthalmol Vis Sci, 2018, 59(2): 715-721. DOI: 10.1167/iovs.17-23042.
26. Landmann R, Müller B, Zimmerli W. CD14, new aspects of ligand and signal diversity[J]. Microbes Infect, 2000, 2(3): 295-304. DOI: 10.1016/s1286-4579(00)00298-7.
27. Yin GN, Jeon H, Lee S, et al. Role of soluble CD14 in cerebrospinal fluid as a regulator of glial functions[J]. J Neurosci Res, 2009, 87(11): 2578-2590. DOI: 10.1002/jnr.22081.
28. Ascaso FJ, Huerva V, Grzybowski A. The role of inflammation in the pathogenesis of macular edema secondary to retinal vascular diseases[J/OL]. Mediators Inflamm, 2014, 2014: 432685[2014-07-22]. https://pubmed.ncbi.nlm.nih.gov/25152567/. DOI: 10.1155/2014/432685.
29. Daruich A, Matet A, Moulin A, et al. Mechanisms of macular edema: beyond the surface[J]. Prog Retin Eye Res, 2018, 63: 20-68. DOI: 10.1016/j.preteyeres.2017.10.006.
30. Marmor MF. Mechanisms of fluid accumulation in retinal edema[J]. Doc Ophthalmol, 1999, 97(3-4): 239-249. DOI: 10.1023/a: 1002192829817.
31. Bunt-Milam AH, Saari JC, Klock IB, et al. Zonulae adherentes pore size in the external limiting membrane of the rabbit retina[J]. Invest Ophthalmol Vis Sci, 1985, 26(10): 1377-1380.
32. Gardner TW, Antonetti DA, Barber AJ, et al. Diabetic retinopathy: more than meets the eye[J]. Surv Ophthalmol, 2002, 47(Suppl 2): S253-262. DOI: 10.1016/s0039-6257(02)00387-9.
33. Tso MO, Cunha-Vaz JG, Shih CY, et al. Clinicopathologic study of blood-retinal barrier in experimental diabetes mellitus[J]. Arch Ophthalmol, 1980, 98(11): 2032-2040. DOI: 10.1001/archopht.1980.01020040884020.
34. Cunha-Vaz J, Ashton P, Iezzi R, et al. Sustained delivery fluocinolone acetonide vitreous implants: long-term benefit in patients with chronic diabetic macular edema[J]. Ophthalmology, 2014, 121(10): 1892-1903. DOI: 10.1016/j.ophtha.2014.04.019.
35. Kang JW, Lee H, Chung H, et al. Correlation between optical coherence tomographic hyperreflective foci and visual outcomes after intravitreal bevacizumab for macular edema in branch retinal vein occlusion[J]. Graefe's Arch Clin Exp Ophthalmol, 2014, 252(9): 1413-1421. DOI: 10.1007/s00417-014-2595-5.
36. Chatziralli IP, Sergentanis TN, Sivaprasad S. Hyperreflective foci as an independent visual outcome predictor in macular edema due to retinal vascular diseases treated with intravitreal dexamethasone or ranibizumab[J]. Retina, 2016, 36(12): 2319-2328. DOI: 10.1097/IAE.0000000000001070.
37. Kang JW, Chung H, Chan Kim H. Correlation of optical coherence tomographic hyperreflective foci with visual outcomes in different patterns of diabetic macular edema[J]. Retina, 2016, 36(9): 1630-1639. DOI: 10.1097/IAE.0000000000000995.
38. Hwang HS, Chae JB, Kim JY, et al. Association between hyperreflective dots on spectral-domain optical coherence tomography in macular edema and response to treatment[J]. Invest Ophthalmol Vis Sci, 2017, 58(13): 5958-5967. DOI: 10.1167/iovs.17-22725.
39. Liu S, Wang D, Chen F, et al. Hyperreflective foci in OCT image as a biomarker of poor prognosis in diabetic macular edema patients treating with conbercept in China[J/OL]. BMC Ophthalmol, 2019, 19(1): 157[2019-07-23]. https://pubmed.ncbi.nlm.nih.gov/31337360/. DOI: 10.1186/s12886-019-1168-0.

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