Research status and recent advances of nanophthalmos_Chinese Journal of Ocular Fundus Diseases

Authors：

Tang You ,  Zhang Meixia

West China Hospital of Sichuan University, Chengdu 610041, China;

Corresponding author：

Zhang Meixia, Email: zhang-meixia@126.com

Keywords：

Microphthalmos/genetics; Uveal diseases/complications; Glaucoma; Review

DOI：

10.3760/cma.j.cn511434-20180824-00298

Video：

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Abstract Full text Figures/Tables Video References Cited by

Nanophthalmos is a congenital disorder, which is characterized by small eye without any ocular or systemic malformation. It has autosomal-dominant and recessive forms of inheritance. It manifests as reduced total axial length, high hyperopia and thickened sclera. Nanophthalmos is relatively rare, but at high risk of secondary angle-closure glaucoma, uveal effusion syndrome. It can be spontaneous remission or recurrent, and responses poorly to medication. The effect of systemic glucocorticoid treatment is not ideal. The surgery challenges with very high rate of intra- and post-operative complications such as hemorrhage, choroidal and retinal detachment, malignum glaucoma and uveal effusion, so that the prognosis is poor. It is of great instructive significance to further understand the clinical features, complications and treatment progress and to avoid the missed diagnosis and misdiagnosisi of its complications, and thus choose the right management.

Citation： Tang You, Zhang Meixia. Research status and recent advances of nanophthalmos. Chinese Journal of Ocular Fundus Diseases, 2020, 36(5): 400-403. doi: 10.3760/cma.j.cn511434-20180824-00298 Copy

1.	Vingolo EM, Steindl K, Forte R, et al. Autosomal dominant simple microphthalmos[J]. J Med Genet, 1994, 31(9): 721-725. DOI: 10.1136/jmg.31.9.721.
2.	Jung KI, Yang JW, Lee YC, et al. Cataract surgery in eyes with nanophthalmos and relative anterior microphthalmos[J]. Am J Ophthalmol, 2012, 153(6): 1161-1168. DOI: 10.1016/j.ajo.2011.12.006.
3.	Relhan N, Jalali S, Pehre N, et al. High-hyperopia database, part Ⅰ: clinical characterisation including morphometric (biometric) differentiation of posterior microphthalmos from nanophthalmos[J]. Eye (Lond), 2016, 30(1): 120-126. DOI: 10.1038/eye.2015.206.
4.	Carricondo PC, Andrade T, Prasov L, et al. Nanophthalmos: a review of the clinical spectrum and genetics[J/OL]. J Ophthalmol, 2018, 2018: 2735465[2018-05-09]. http://europepmc.org/article/MED/29862063. DOI: 10.1155/2018/2735465..
5.	Siggs OM, Awadalla MS, Souzeau E. The genetic and clinical landscape of nanophthalmos and posterior microphthalmos in an Australian cohort[J]. Clin Genet, 2020, 97(5): 764-769. DOI: 10.1111/cge.13722.
6.	Sundin OH, Leppert GS, Silva ED, et al. Extreme hyperopia is the result of null mutations in MFRP, which encodes a frizzled-related protein[J]. Proc Natl Acad Sci USA, 2005, 102(27): 9553-9558. DOI: 10.1073/pnas.0501451102.
7.	Gal A, Rau I, El Matri L, et al. Autosomal-recessive posterior microphthalmos is caused by mutations in PRSS56, a gene encoding a trypsin-like serine protease[J]. Am J Hum Genet, 2011, 88(3): 382-390. DOI: 10.1016/j.ajhg.2011.02.006.
8.	Orr A, Dube MP, Zenteno JC, et al. Mutations in a novel serine protease PRSS56 in families with nanophthalmos[J]. Mol Vis, 2011, 17: 1850-1861.
9.	Sundin OH, Dharmaraj S, Bhutto IA, et al. Developmental basis of nanophthalmos: MFRP is required for both prenatal ocular growth and postnatal emmetropization[J]. Ophthalmic Genet, 2008, 29(1): 1-9. DOI: 10.1080/13816810701651241.
10.	Nair KS, Hmani-Aifa M, Ali Z, et al. Alteration of the serine protease PRSS56 causes angle-closure glaucoma in mice and posterior microphthalmia in humans and mice[J]. Nat Genet, 2011, 43(6): 579-584. DOI: 10.1038/ng.813.
11.	Awadalla MS, Burdon KP, Souzeau E, et al. Mutation in TMEM98 in a large white kindred with autosomal dominant nanophthalmos linked to 17p12-q12[J]. JAMA Ophthalmol, 2014, 132(8): 970-977. DOI: 10.1001/jamaophthalmol.2014.946.
12.	Khorram D, Choi M, Roos BR, et al. Novel TMEM98 mutations in pedigrees with autosomal dominant nanophthalmos[J]. Mol Vis, 2015, 21: 1017-1023.
13.	Cross SH, McKie L, Keighren M, et al. Missense mutations in the human nanophthalmos gene TMEM98 cause retinal defects in the mouse[J]. Invest Ophthalmol Vis Sci, 2019, 60(8): 2875-2887. DOI: 10.1167/iovs.18-25954.
14.	Othman MI, Sullivan SA, Skuta GL, et al. Autosomal dominant nanophthalmos (NNO1) with high hyperopia and angle-closure glaucoma maps to chromosome 11[J]. Am J Hum Genet, 1998, 63(5): 1411-1418. DOI: 10.1086/302113.
15.	Garnai SJ, Brinkmeier ML, Emery B, et al. Variants in myelin regulatory factor (MYRF) cause autosomal dominant and syndromic nanophthalmos in humans and retinal degeneration in mice[J/OL]. PLoS Genet, 2019, 15(5): 1008130[2019-05-02]. http://europepmc.org/article/MED/31048900. DOI: 10.1371/journal.pgen.1008130.
16.	Guo C, Zhao Z, Chen D, et al. Detection of clinically relevant genetic variants in Chinese patients with nanophthalmos by trio-based whole-genome sequencing study[J]. Invest Ophthalmol Vis Sci, 2019, 60(8): 2904-2913. DOI: 10.1167/iovs.18-26275.
17.	Pinz H, Pyle LC, Li D, et al. De novo variants in myelin regulatory factor (MYRF) as candidates of a new syndrome of cardiac and urogenital anomalies[J]. Am J Med Genet A, 2018, 176(4): 969-972. DOI: 10.1002/ajmg.a.38620.
18.	Rossetti LZ, Glinton K, Yuan B, et al. Review of the phenotypic spectrum associated with haploinsufficiency of MYRF[J]. Am J Med Genet A, 2019, 179(7): 1376-1382. DOI: 10.1002/ajmg.a.61182.
19.	Huang H, Teng P, Du J, et al. Interactive repression of MYRF self-cleavage and activity in oligodendrocyte differentiation by TMEM98 protein[J]. J Neurosci, 2018, 38(46): 9829-9839. DOI: 10.1523/jneurosci.0154-18.2018.
20.	Yardley J, Leroy BP, Hart-Holden N, et al. Mutations of VMD2 splicing regulators cause nanophthalmos and autosomal dominant vitreoretinochoroidopathy (ADVIRC)[J]. Invest Ophthalmol Vis Sci, 2004, 45(10): 3683-3689. DOI: 10.1167/iovs.04-0550.
21.	Zenteno JC, Buentello-Volante B, Ayala-Ramirez R, et al. Homozygosity mapping identifies the crumbs homologue 1(Crb1) gene as responsible for a recessive syndrome of retinitis pigmentosa and nanophthalmos[J]. Am J Med Genet A, 2011, 155A(5): 1001-1006. DOI: 10.1002/ajmg.a.33862.
22.	Li H, Wang JX, Wang CY, et al. Localization of a novel gene for congenital nonsyndromic simple microphthalmia to chromosome 2q11-14[J]. Human Genetics, 2008, 122(6): 589-593. DOI: 10.1007/s00439-007-0435-y.
23.	Duke-Elder S. Normal and abnormal development[M]//Duke-Elder S. System of ophthalmology. St Louis: Mosby, 1964: 488-495.
24.	Weiss AH, Kousseff BG, Ross EA, et al. Simple microphthalmos[J]. Arch Ophthalmol, 1989, 107(11): 1625-1630. DOI: 10.1001/archopht.1989.01070020697031.
25.	Zheng T, Chen Z, Xu J, et al. Outcomes and prognostic factors of cataract surgery in adult extreme microphthalmos with axial length<18 mm or corneal diameter<8 mm[J]. Am J Ophthalmol, 2017, 184: 84-96. DOI: 10.1016/j.ajo.2017.09.028.
26.	Spitznas M, Gerke E, Bateman JB. Hereditary posterior microphthalmos with papillomacular fold and high hyperopia[J]. Arch Ophthalmol, 1983, 101(3): 413-417. DOI: 10.1001/archopht.1983.01040010413014.
27.	Brockhurst RJ. Nanophthalmos with uveal effusion: a new clinical entity[J]. Arch Ophthalmol, 1975, 93(12): 1989-1999. DOI: 10.1001/archopht.1975.01010020923001.
28.	Uyama M, Takahashi K, Kozaki J, et al. Uveal effusion syndrome: clinical features, surgical treatment, histologic examination of the sclera, and pathophysiology[J]. Ophthalmology, 2000, 107(3): 441-449. DOI: 10.1016/s0161-6420(99)00141-4.
29.	Forrester JV, Lee WR, Kerr PR, et al. The uveal effusion syndrome and trans-scleral flow[J]. Eye (Lond), 1990, 4(t2): 354-365. DOI: 10.1038/eye.1990.48.
30.	Demircan A, Yesilkaya C, Altan C, et al. Foveal avascular zone area measurements with optical coherence tomography angiography in patients with nanophthalmos[J]. Eye (Lond), 2019, 33(3): 445-450. DOI: 10.1038/s41433-018-0236-7.
31.	Yalvac IS, Satana B, Ozkan G, et al. Management of glaucoma in patients with nanophthalmos[J]. Eye (Lond), 2008, 22(6): 838-843. DOI: 10.1038/sj.eye.6702742.
32.	Altintas AK, Acar MA, Yalvac IS, et al. Autosomal recessive nanophthalmos[J]. Acta Ophthalmol Scand, 1997, 75(3): 325-328. DOI: 10.1111/j.1600-0420.1997.tb00788.x.
33.	王华, 唐炘, 王涛. 拉坦前列素滴眼液治疗真性小眼球继发闭角型青光眼的疗效观察[J]. 中国实用眼科杂志, 2011, 29(8): 772-774. DOI: 10.3760/cma.j.issn.1006-4443.2011.08.007.Wang H, Tang X, Wang T. The effect of latanoproston the treatment of nanophthalmos combined with angle closure glaucoma[J]. Chin J Pract Ophthalmol, 2011, 29(8): 772-774. DOI: 10.3760/cma.j.issn.1006-4443.2011.08.007.
34.	余敏斌, 黄圣松, 叶天才. 真性小眼球继发青光眼的治疗[J]. 中国实用眼科杂志, 2002, 20(9): 677-679. DOI: 10.3760/cma.j.issn.1006-4443.2002.09.012.Yu MB, Huang SS, Ye TC. The management of glaucoma in nanophthalmic patients[J]. Chin J Pract Ophthalmol, 2002, 20(9): 677-679. DOI: 10.3760/cma.j.issn.1006-4443.2002.09.012.
35.	Burgoyne C, Tello C, Katz LJ. Nanophthalmia and chronic angle-closure glaucoma[J]. J Glaucoma, 2002, 11(6): 525-528. DOI: 10.1097/00061198-200212000-00013.
36.	Elagouz M, Stanescu-Segall D, Jackson TL. Uveal effusion syndrome[J]. Surv Ophthalmol, 2010, 55(2): 134-145. DOI: 10.1016/j.survophthal.2009.05.003.
37.	黎铧, 李娟娟, 王萍, 等. 脉络膜渗漏综合征多种眼底影像特征对比观察[J]. 中华眼底病杂志, 2016, 32(6): 639-641. DOI: 10.3760/cma.j.issn.1005-1015.2016.06.018.Li Y, Li JJ, Wang P, et al. Contrastive observation of fundus image characteristics of choroidal leakage syndrome[J]. Chin J Ocul Fundus Dis, 2016, 32(6): 639-641. DOI: 10.3760/cma.j.issn.1005-1015.2016.06.018.
38.	Gass JD. Uveal effusion syndrome: a new hypothesis concerning pathogenesis and technique of surgical treatment[J]. Retina, 1983, 3(3): 159-163. DOI: 10.1097/00006982-198300330-00003.
39.	Besirli CG, Johnson MW. Uveal effusion syndrome and hypotony maculopathy[M]//Stephen JR. Retina. 5th ed. Philadelphia: Saunders, 2013: 1306-1317.
40.	Mansour A, Stewart MW, Shields CL. Extensive circumferential partial-thickness sclerectomy in eyes with extreme nanophthalmos and spontaneous uveal effusion[J]. Br J Ophthalmol, 2019, 103(12): 1862-1867. DOI: 10.1136/bjophthalmol-2018-313702.
41.	Khatri A, Singh S, Joshi K, et al. Quadrantic vortex vein decompression with subretinal fluid drainage for manangement of Nanophthalmic choroidal effusions: a review of literature and case series[J]. BMC Ophthalmol, 2019, 19(1): 210. DOI: 10.1186/s12886-019-1213-z.

1. Vingolo EM, Steindl K, Forte R, et al. Autosomal dominant simple microphthalmos[J]. J Med Genet, 1994, 31(9): 721-725. DOI: 10.1136/jmg.31.9.721.
2. Jung KI, Yang JW, Lee YC, et al. Cataract surgery in eyes with nanophthalmos and relative anterior microphthalmos[J]. Am J Ophthalmol, 2012, 153(6): 1161-1168. DOI: 10.1016/j.ajo.2011.12.006.
3. Relhan N, Jalali S, Pehre N, et al. High-hyperopia database, part Ⅰ: clinical characterisation including morphometric (biometric) differentiation of posterior microphthalmos from nanophthalmos[J]. Eye (Lond), 2016, 30(1): 120-126. DOI: 10.1038/eye.2015.206.
4. Carricondo PC, Andrade T, Prasov L, et al. Nanophthalmos: a review of the clinical spectrum and genetics[J/OL]. J Ophthalmol, 2018, 2018: 2735465[2018-05-09]. http://europepmc.org/article/MED/29862063. DOI: 10.1155/2018/2735465..
5. Siggs OM, Awadalla MS, Souzeau E. The genetic and clinical landscape of nanophthalmos and posterior microphthalmos in an Australian cohort[J]. Clin Genet, 2020, 97(5): 764-769. DOI: 10.1111/cge.13722.
6. Sundin OH, Leppert GS, Silva ED, et al. Extreme hyperopia is the result of null mutations in MFRP, which encodes a frizzled-related protein[J]. Proc Natl Acad Sci USA, 2005, 102(27): 9553-9558. DOI: 10.1073/pnas.0501451102.
7. Gal A, Rau I, El Matri L, et al. Autosomal-recessive posterior microphthalmos is caused by mutations in PRSS56, a gene encoding a trypsin-like serine protease[J]. Am J Hum Genet, 2011, 88(3): 382-390. DOI: 10.1016/j.ajhg.2011.02.006.
8. Orr A, Dube MP, Zenteno JC, et al. Mutations in a novel serine protease PRSS56 in families with nanophthalmos[J]. Mol Vis, 2011, 17: 1850-1861.
9. Sundin OH, Dharmaraj S, Bhutto IA, et al. Developmental basis of nanophthalmos: MFRP is required for both prenatal ocular growth and postnatal emmetropization[J]. Ophthalmic Genet, 2008, 29(1): 1-9. DOI: 10.1080/13816810701651241.
10. Nair KS, Hmani-Aifa M, Ali Z, et al. Alteration of the serine protease PRSS56 causes angle-closure glaucoma in mice and posterior microphthalmia in humans and mice[J]. Nat Genet, 2011, 43(6): 579-584. DOI: 10.1038/ng.813.
11. Awadalla MS, Burdon KP, Souzeau E, et al. Mutation in TMEM98 in a large white kindred with autosomal dominant nanophthalmos linked to 17p12-q12[J]. JAMA Ophthalmol, 2014, 132(8): 970-977. DOI: 10.1001/jamaophthalmol.2014.946.
12. Khorram D, Choi M, Roos BR, et al. Novel TMEM98 mutations in pedigrees with autosomal dominant nanophthalmos[J]. Mol Vis, 2015, 21: 1017-1023.
13. Cross SH, McKie L, Keighren M, et al. Missense mutations in the human nanophthalmos gene TMEM98 cause retinal defects in the mouse[J]. Invest Ophthalmol Vis Sci, 2019, 60(8): 2875-2887. DOI: 10.1167/iovs.18-25954.
14. Othman MI, Sullivan SA, Skuta GL, et al. Autosomal dominant nanophthalmos (NNO1) with high hyperopia and angle-closure glaucoma maps to chromosome 11[J]. Am J Hum Genet, 1998, 63(5): 1411-1418. DOI: 10.1086/302113.
15. Garnai SJ, Brinkmeier ML, Emery B, et al. Variants in myelin regulatory factor (MYRF) cause autosomal dominant and syndromic nanophthalmos in humans and retinal degeneration in mice[J/OL]. PLoS Genet, 2019, 15(5): 1008130[2019-05-02]. http://europepmc.org/article/MED/31048900. DOI: 10.1371/journal.pgen.1008130.
16. Guo C, Zhao Z, Chen D, et al. Detection of clinically relevant genetic variants in Chinese patients with nanophthalmos by trio-based whole-genome sequencing study[J]. Invest Ophthalmol Vis Sci, 2019, 60(8): 2904-2913. DOI: 10.1167/iovs.18-26275.
17. Pinz H, Pyle LC, Li D, et al. De novo variants in myelin regulatory factor (MYRF) as candidates of a new syndrome of cardiac and urogenital anomalies[J]. Am J Med Genet A, 2018, 176(4): 969-972. DOI: 10.1002/ajmg.a.38620.
18. Rossetti LZ, Glinton K, Yuan B, et al. Review of the phenotypic spectrum associated with haploinsufficiency of MYRF[J]. Am J Med Genet A, 2019, 179(7): 1376-1382. DOI: 10.1002/ajmg.a.61182.
19. Huang H, Teng P, Du J, et al. Interactive repression of MYRF self-cleavage and activity in oligodendrocyte differentiation by TMEM98 protein[J]. J Neurosci, 2018, 38(46): 9829-9839. DOI: 10.1523/jneurosci.0154-18.2018.
20. Yardley J, Leroy BP, Hart-Holden N, et al. Mutations of VMD2 splicing regulators cause nanophthalmos and autosomal dominant vitreoretinochoroidopathy (ADVIRC)[J]. Invest Ophthalmol Vis Sci, 2004, 45(10): 3683-3689. DOI: 10.1167/iovs.04-0550.
21. Zenteno JC, Buentello-Volante B, Ayala-Ramirez R, et al. Homozygosity mapping identifies the crumbs homologue 1(Crb1) gene as responsible for a recessive syndrome of retinitis pigmentosa and nanophthalmos[J]. Am J Med Genet A, 2011, 155A(5): 1001-1006. DOI: 10.1002/ajmg.a.33862.
22. Li H, Wang JX, Wang CY, et al. Localization of a novel gene for congenital nonsyndromic simple microphthalmia to chromosome 2q11-14[J]. Human Genetics, 2008, 122(6): 589-593. DOI: 10.1007/s00439-007-0435-y.
23. Duke-Elder S. Normal and abnormal development[M]//Duke-Elder S. System of ophthalmology. St Louis: Mosby, 1964: 488-495.
24. Weiss AH, Kousseff BG, Ross EA, et al. Simple microphthalmos[J]. Arch Ophthalmol, 1989, 107(11): 1625-1630. DOI: 10.1001/archopht.1989.01070020697031.
25. Zheng T, Chen Z, Xu J, et al. Outcomes and prognostic factors of cataract surgery in adult extreme microphthalmos with axial length<18 mm or corneal diameter<8 mm[J]. Am J Ophthalmol, 2017, 184: 84-96. DOI: 10.1016/j.ajo.2017.09.028.
26. Spitznas M, Gerke E, Bateman JB. Hereditary posterior microphthalmos with papillomacular fold and high hyperopia[J]. Arch Ophthalmol, 1983, 101(3): 413-417. DOI: 10.1001/archopht.1983.01040010413014.
27. Brockhurst RJ. Nanophthalmos with uveal effusion: a new clinical entity[J]. Arch Ophthalmol, 1975, 93(12): 1989-1999. DOI: 10.1001/archopht.1975.01010020923001.
28. Uyama M, Takahashi K, Kozaki J, et al. Uveal effusion syndrome: clinical features, surgical treatment, histologic examination of the sclera, and pathophysiology[J]. Ophthalmology, 2000, 107(3): 441-449. DOI: 10.1016/s0161-6420(99)00141-4.
29. Forrester JV, Lee WR, Kerr PR, et al. The uveal effusion syndrome and trans-scleral flow[J]. Eye (Lond), 1990, 4(t2): 354-365. DOI: 10.1038/eye.1990.48.
30. Demircan A, Yesilkaya C, Altan C, et al. Foveal avascular zone area measurements with optical coherence tomography angiography in patients with nanophthalmos[J]. Eye (Lond), 2019, 33(3): 445-450. DOI: 10.1038/s41433-018-0236-7.
31. Yalvac IS, Satana B, Ozkan G, et al. Management of glaucoma in patients with nanophthalmos[J]. Eye (Lond), 2008, 22(6): 838-843. DOI: 10.1038/sj.eye.6702742.
32. Altintas AK, Acar MA, Yalvac IS, et al. Autosomal recessive nanophthalmos[J]. Acta Ophthalmol Scand, 1997, 75(3): 325-328. DOI: 10.1111/j.1600-0420.1997.tb00788.x.
33. 王华, 唐炘, 王涛. 拉坦前列素滴眼液治疗真性小眼球继发闭角型青光眼的疗效观察[J]. 中国实用眼科杂志, 2011, 29(8): 772-774. DOI: 10.3760/cma.j.issn.1006-4443.2011.08.007.Wang H, Tang X, Wang T. The effect of latanoproston the treatment of nanophthalmos combined with angle closure glaucoma[J]. Chin J Pract Ophthalmol, 2011, 29(8): 772-774. DOI: 10.3760/cma.j.issn.1006-4443.2011.08.007.
34. 余敏斌, 黄圣松, 叶天才. 真性小眼球继发青光眼的治疗[J]. 中国实用眼科杂志, 2002, 20(9): 677-679. DOI: 10.3760/cma.j.issn.1006-4443.2002.09.012.Yu MB, Huang SS, Ye TC. The management of glaucoma in nanophthalmic patients[J]. Chin J Pract Ophthalmol, 2002, 20(9): 677-679. DOI: 10.3760/cma.j.issn.1006-4443.2002.09.012.
35. Burgoyne C, Tello C, Katz LJ. Nanophthalmia and chronic angle-closure glaucoma[J]. J Glaucoma, 2002, 11(6): 525-528. DOI: 10.1097/00061198-200212000-00013.
36. Elagouz M, Stanescu-Segall D, Jackson TL. Uveal effusion syndrome[J]. Surv Ophthalmol, 2010, 55(2): 134-145. DOI: 10.1016/j.survophthal.2009.05.003.
37. 黎铧, 李娟娟, 王萍, 等. 脉络膜渗漏综合征多种眼底影像特征对比观察[J]. 中华眼底病杂志, 2016, 32(6): 639-641. DOI: 10.3760/cma.j.issn.1005-1015.2016.06.018.Li Y, Li JJ, Wang P, et al. Contrastive observation of fundus image characteristics of choroidal leakage syndrome[J]. Chin J Ocul Fundus Dis, 2016, 32(6): 639-641. DOI: 10.3760/cma.j.issn.1005-1015.2016.06.018.
38. Gass JD. Uveal effusion syndrome: a new hypothesis concerning pathogenesis and technique of surgical treatment[J]. Retina, 1983, 3(3): 159-163. DOI: 10.1097/00006982-198300330-00003.
39. Besirli CG, Johnson MW. Uveal effusion syndrome and hypotony maculopathy[M]//Stephen JR. Retina. 5th ed. Philadelphia: Saunders, 2013: 1306-1317.
40. Mansour A, Stewart MW, Shields CL. Extensive circumferential partial-thickness sclerectomy in eyes with extreme nanophthalmos and spontaneous uveal effusion[J]. Br J Ophthalmol, 2019, 103(12): 1862-1867. DOI: 10.1136/bjophthalmol-2018-313702.
41. Khatri A, Singh S, Joshi K, et al. Quadrantic vortex vein decompression with subretinal fluid drainage for manangement of Nanophthalmic choroidal effusions: a review of literature and case series[J]. BMC Ophthalmol, 2019, 19(1): 210. DOI: 10.1186/s12886-019-1213-z.

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