Biomechanical Factors in Space Flight-Associated Neuro-Ocular Syndrome
Wang Xiaofei1,2,3#, Liu Tingting1,2,3, Fan Yubo1,2,3#*
1(Key Laboratory for Biomechanics and Mechanobiology of Ministry of Education, Beijing 100083, China) 2(Beijing Advanced Innovation Center for Biomedical Engineering, Beijing 100083, China) 3(School of Biological Science and Medical Engineering, Beihang University, Beijing 100083, China)
Abstract：Long duration space flight can induce structural changes of eye and corresponding vision loss, which is defined as space flight-associated neuro-ocular syndrome (SANS). SANS is the main problem of eye for future human space exploration. Up to date, mechanisms of SANS are still unknown, which impedes the development of countermeasures and the selection criteria of astronauts. SANS is correlated with optic nerve subarachnoid space cerebrospinal fluid pressure elevation in microgravity environments. However, knowledge on the detailed response of eyes to elevated pressure and its corresponding countermeasures is lack. This paper summarized the morphological changes of the optic disc, posterior segment of the eye, subarachnoid space and optic nerve caused by SANS. Next, the pathogenesis of SANS proposed in the literature, the factors affecting the susceptibility of SANS and the countermeasures were reviewed and the relationship between SANS and the optic nerve subarachnoid space cerebrospinal fluid pressure in microgravity environment was summarized. At last, we discussed how to effectively combine ground-based and space-based experiments to explore the pathogenesis of SANS.
作者简介: #中国生物医学工程学会会员(Member, Chinese Society of Biomedical Engineering)
引用本文:
王晓飞, 刘亭亭, 樊瑜波. 太空飞行神经眼综合征的生物力学因素研究进展[J]. 中国生物医学工程学报, 2022, 41(4): 493-501.
Wang Xiaofei, Liu Tingting, Fan Yubo. Biomechanical Factors in Space Flight-Associated Neuro-Ocular Syndrome. Chinese Journal of Biomedical Engineering, 2022, 41(4): 493-501.
[1] Garrett-Bakelman FE, Darshi M, Green SJ, et al. The nasa twins study: a multidimensional analysis of a year-long human spaceflight[J]. Science, 2019, 364(6436): eaau8650. [2] Mader TH, Gibson CR, Pass AF, et al. Optic disc edema, globe flattening, choroidal folds, and hyperopic shifts observed in astronauts after long-duration space flight[J]. Ophthalmology, 2011, 118(10): 2058-2069. [3] Lee AG, Mader TH, Gibson CR, et al. Space flight-associated neuro-ocular syndrome[J]. JAMA Ophthalmology, 2017, 135(9): 992-994. [4] Zhang Lifan, Hargens AR. Spaceflight-induced intracranial hypertension and visual impairment: pathophysiology and countermeasures[J]. Physiological Reviews, 2018, 98(1): 59-87. [5] Lee AG, Tarver WJ, Mader TH, et al. Neuro-ophthalmology of space flight[J]. Journal of Neuro-Ophthalmology, 2016, 36(1): 85-91. [6] Afshinnekoo E, Scott RT, MacKay MJ, et al. Fundamental biological features of spaceflight: advancing the field to enable deep-space exploration[J]. Cell, 2020, 183(5): 1162-1184. [7] Wostyn P, Winne DF, Stern C, et al. Dilated prelaminar paravascular spaces as a possible mechanism for optic disc edema in astronauts[J]. Aerospace Medicine and Human Performance, 2018, 89(12): 1089-1091. [8] Huang AS, Stenger MB, Macias BR. Gravitational influence on intraocular pressure: implications for spaceflight and disease[J]. Journal of Glaucoma, 2019, 28(8): 756-764. [9] Feola AJ, Coudrillier B, Mulvihill J, et al. Deformation of the lamina cribrosa and optic nerve due to changes in cerebrospinal fluid pressure[J]. Investigative Ophthalmology & Visual Science, 2017, 58(4): 2070-2078. [10] Lee AG, Mader TH, Gibson CR, et al. Spaceflight associated neuro-ocular syndrome (sans) and the neuro-ophthalmologic effects of microgravity: a review and an update[J]. NPJ Microgravity, 2020, 6(1): 23. [11] Lee C, Rohr J, Sass A, et al. In vivo estimation of optic nerve sheath stiffness using noninvasive MRI measurements and finite element modeling[J]. Journal of the Mechanical Behavior of Biomedical Materials, 2020, 110: 103924. [12] Alperin N, Bagci AM, Oliu CJ, et al. Role of cerebrospinal fluid in spaceflight-induced ocular changes and visual impairment in astronauts[J]. Radiology, 2017, 285(3): 1063. [13] Alperin N, Bagci AM. Spaceflight-induced visual impairment and globe deformations in astronauts are linked to orbital cerebrospinal fluid volume increase[M]//Intracranial Pressure & Neuromonitoring XVI. Cham: Springer International Publishing, 2018: 215-219. [14] 张晨晨, 李佳, 牛灵芝, 等. 微重力环境引起宇航员眼部改变及其机制的研究进展[J]. 中华眼视光学与视觉科学杂志, 2020, 22(1): 72-77. [15] 赵军, 胡莲娜, 李志生, 等. 头低位模拟失重对正常人视觉诱发电位的影响[J]. 眼科新进展, 2009(10): 756-758. [16] Bock O, Weigelt C, Bloomberg JJ. Cognitive demand of human sensorimotor performance during an extended space mission: a dual-task study[J]. Aviation, Space, and Environmental Medicine, 2010, 81(9): 819-824. [17] Kramer LA, Sargsyan AE, Hasan KM, et al. Orbital and intracranial effects of microgravity: findings at 3-T MR imaging[J]. Radiology, 2012, 263(3): 819-827. [18] Mader TH, Gibson CR, Barratt MR, et al. Persistent globe flattening in astronauts following long-duration spaceflight[J]. Neuro-Ophthalmology, 2021, 45(1): 29-35. [19] Rohr JJ, Sater S, Sass AM, et al. Quantitative magnetic resonance image assessment of the optic nerve and surrounding sheath after spaceflight[J]. NPJ Microgravity, 2020, 6: 30. [20] Wåhlin A, Holmlund P, Fellows AM, et al. Optic nerve length before and after spaceflight[J]. Ophthalmology, 2020,128(2):309-316. [21] Roberts DR, Albrecht MH, Collins HR, et al. Effects of spaceflight on astronaut brain structure as indicated on MRI[J]. New England Journal of Medicine, 2017, 377(18): 1746-1753. [22] Ombergen VA, Jillings S, Jeurissen B, et al. Brain ventricular volume changes induced by long-duration spaceflight[J]. Proceedings of the National Academy of Sciences, 2019, 116(21): 10531-10536. [23] Roberts DR, Brown TR, Nietert PJ, et al. Prolonged microgravity affects human brain structure and function[J]. American Journal of Neuroradiology, 2019, 40(11): 1878-1885. [24] Hupfeld KE, McGregor HR, Lee JK, et al. The impact of 6 and 12 months in space on human brain structure and intracranial fluid shifts[J]. Cerebral Cortex Communications, 2020, 1(1): tgaa023. [25] Mader TH, Gibson CR, Otto CA, et al. Persistent asymmetric optic disc swelling after long-duration space flight: implications for pathogenesis[J]. Journal of Neuro-Ophthalmology, 2017, 37(2): 133-139. [26] Patel N, Pass A, Mason S, et al. Optical coherence tomography analysis of the optic nerve head and surrounding structures in long-duration international space station astronauts[J]. JAMA Ophthalmology, 2018, 136(2): 193-200. [27] Laurie SS, Lee SMC, Macias BR, et al. Optic disc edema and choroidal engorgement in astronauts during spaceflight and individuals exposed to bed rest[J]. JAMA Ophthalmology, 2020, 138(2): 165-172. [28] Macias BR, Patel NB, Gibson CR, et al. Association of long-duration spaceflight with anterior and posterior ocular structure changes in astronauts and their recovery[J]. JAMA Ophthalmology, 2020, 138(5): 553-559. [29] Andresen M, Hadi A, Petersen LG, et al. Effect of postural changes on icp in healthy and ill subjects[J]. Acta Neurochirurgica, 2015, 157(1): 109-113. [30] Rasmussen JC, Kwon S, Pinal A, et al. Assessing lymphatic route of csf outflow and peripheral lymphatic contractile activity during head-down tilt using near-infrared fluorescence imaging[J]. Physiological Reports, 2020, 8(4): e14375. [31] Lawley JS, Petersen LG, Howden EJ, et al. Effect of gravity and microgravity on intracranial pressure[J]. The Journal of Physiology, 2017, 595(6): 2115-2127. [32] Zwart SR, Gibson CR, Mader TH, et al. Vision changes after spaceflight are related to alterations in folate-and Vitamin B-12-dependent one-carbon metabolism[J]. The Journal of Nutrition, 2012, 142(3): 427-431. [33] Law J, Van Baalen M, Foy M, et al. Relationship between carbon dioxide levels and reported headaches on the international space station[J]. Journal of Occupational and Environmental Medicine, 2014, 56(5): 477-483. [34] Kurazumi T, Ogawa Y, Yanagida R, et al. Non-invasive intracranial pressure estimation during combined exposure to CO2 and head-down tilt[J]. Aerospace Medicine and Human Performance, 2018, 89(4): 365-370. [35] Marshall-Bowman K, Barratt MR, Gibson CR. Ophthalmic changes and increased intracranial pressure associated with long duration spaceflight: an emerging understanding[J]. Acta Astronautica, 2013, 87: 77-87. [36] Killer HE, Laeng HR, Flammer J, et al. Architecture of arachnoid trabeculae, pillars, and septa in the subarachnoid space of the human optic nerve: anatomy and clinical considerations[J]. British Journal of Ophthalmology, 2003, 87(6): 777-781. [37] Liugan M, Xu Zhaoyang, Zhang Ming. Reduced free communication of the subarachnoid space within the optic canal in the human[J]. American Journal of Ophthalmology, 2017, 179: 25-31. [38] Killer HE, Jaggi GP, Flammer J, et al. The optic nerve: a new window into cerebrospinal fluid composition?[J]. Brain, 2006, 129(4): 1027-1030. [39] Hou R, Zhang Z, Yang D, et al. Intracranial pressure (ICP) and optic nerve subarachnoid space pressure (ONSP) correlation in the optic nerve chamber: the beijing intracranial and intraocular pressure (ICOP) study[J]. Brain Research, 2016, 1635: 201-208. [40] Nelson ES, Mulugeta L, Feola A, et al. The impact of ocular hemodynamics and intracranial pressure on intraocular pressure during acute gravitational changes[J]. Journal of Applied Physiology, 2017, 123(2): 352-363. [41] Yang D, Fu J, Hou R, et al. Optic neuropathy induced by experimentally reduced cerebrospinal fluid pressure in monkeys[J]. Investigative Ophthalmology & Visual Science, 2014, 55(5): 3067-3073. [42] Morgan WH, Chauhan BC, Yu Daoyi, et al. Optic disc movement with variations in intraocular and cerebrospinal fluid pressure[J]. Investigative Ophthalmology & Visual Science, 2002, 43(10): 3236-3242. [43] Wang B, Tran H, Smith MA, et al. In-vivo effects of intraocular and intracranial pressures on the lamina cribrosa microstructure[J]. PLoS ONE, 2017, 12(11): e0188302. [44] Fazio MA, Clark ME, Bruno L, et al. In vivo optic nerve head mechanical response to intraocular and cerebrospinal fluid pressure: imaging protocol and quantification method[J]. Scientific Reports, 2018, 8(1): 12639. [45] Taibbi G, Cromwell RL, Zanello SB, et al. Ocular outcomes comparison between 14-and 70-day head-down-tilt bed rest[J]. Investigative Ophthalmology & Visual Science, 2016, 57(2): 495-501. [46] Taibbi G, Cromwell RL, Zanello SB, et al. Ophthalmological evaluation of integrated resistance and aerobic training during 70-day bed rest[J]. Aerospace Medicine and Human Performance, 2017, 88(7): 633-640. [47] Laurie SS, Macias BR, Dunn JT, et al. Optic disc edema after 30 days of strict head-down tilt bed rest[J]. Ophthalmology, 2019, 126(3): 467-468. [48] Wang Xiaofei, Beotra MR, Tun TA, et al. In vivo 3-dimensional strain mapping confirms large optic nerve head deformations following horizontal eye movements[J]. Investigative Ophthalmology & Visual Science, 2016, 57(13): 5825-5833. [49] Girard MJ A, Beotra MR, Chin KS, et al. In Vivo 3-dimensional strain mapping of the optic nerve head following intraocular pressure lowering by trabeculectomy[J]. Ophthalmology, 6, 123(6): 1190-1200. [50] Sigal IA, Flanagan JG, Tertinegg I, et al. Modeling individual-specific human optic nerve head biomechanics. Part ii: influence of material properties[J]. Biomechanics and Modeling in Mechanobiology, 2009, 8(2): 99-109. [51] Liu Baiyun, McNally S, Kilpatrick JI, et al. Aging and ocular tissue stiffness in glaucoma[J]. Survey of Ophthalmology, 2018, 63(1): 56-74. [52] Downs JC. Optic nerve head biomechanics in aging and disease[J]. Experimental Eye Research, 2015, 133: 19-29. [53] Zhang Liang, Albon J, Jones H, et al. Collagen microstructural factors influencing optic nerve head biomechanics[J]. Investigative Ophthalmology & Visual Science, 2015, 56(3): 2031-2042. [54] Wang Xiaofei, Fisher LK, Milea D, et al. Predictions of optic nerve traction forces and peripapillary tissue stresses following horizontal eye movements[J]. Investigative Ophthalmology & Visual Science, 2017, 58(4): 2044-2053. [55] Wang Xiaofei, Rumpel H, Lim WEH, et al. Finite element analysis predicts large optic nerve head strains during horizontal eye movements[J]. Investigative Ophthalmology & Visual Science, 2016, 57(6): 2452-2462. [56] Hua Yi, Voorhees AP, Sigal IA. Cerebrospinal fluid pressure: revisiting factors influencing optic nerve head biomechanics[J]. Investigative Opthalmology & Visual Science, 2018, 59(1): 154-165. [57] Feola AJ, Myers JG, Raykin J, et al. Finite element modeling of factors influencing optic nerve head deformation due to intracranial pressure[J]. Investigative Ophthalmology & Visual Science, 2016, 57(4): 1901-1911. [58] Hansen HC, Helmke K. Validation of the optic nerve sheath response to changing cerebrospinal fluid pressure: ultrasound findings during intrathecal infusion tests[J]. Journal of Neurosurgery, 1997, 87(1): 34-40. [59] Wostyn P, De Deyn PP. Intracranial pressure-induced optic nerve sheath response as a predictive biomarker for optic disc edema in astronauts[J]. Biomarkers in Medicine, 2017, 11(11): 1003-1008. [60] Wostyn P, Mader TH, Gibson CR, et al. The possible role of elastic properties of the brain and optic nerve sheath in the development of spaceflight-associated neuro-ocular syndrome[J]. American Journal of Neuroradiology, 2020, 41(3): E14-E15. [61] Wostyn P, De Deyn PP. Optic nerve sheath distention as a protective mechanism against the visual impairment and intracranial pressure syndrome in astronauts[J]. Investigative Ophthalmology & Visual Science, 2017, 58(11): 4601-4602. [62] Raykin J, Forte TE, Wang Roy, et al. Characterization of the mechanical behavior of the optic nerve sheath and its role in spaceflight-induced ophthalmic changes[J]. Biomechanics and Modeling in Mechanobiology, 2017, 16(1): 33-43. [63] Scott JM, Charles JB. Lower body negative pressure as a VIIP countermeasure[M]//Intracranial Pressure and its Effect on Vision in Space and on Earth. Singapore City: World Scientific, 2017: 253-271. [64] Marshall-Goebel K, Laurie SS, Alferova IV, et al. Assessment of jugular venous blood flow stasis and thrombosis during spaceflight[J]. JAMA Network Open, 2019, 2(11): e1915011. [65] Yarmanova EN, Kozlovskaya IB, Khimoroda N, et al. Evolution of Russian microgravity countermeasures[J]. Aerosp Med Hum Perform, 2015, 86(12 Suppl): A32-A37. [66] Ashari N, Hargens AR. The mobile lower body negative pressure gravity suit for long-duration spaceflight[J]. Frontiers in Physiology, 2020, 11: 997. [67] Scott JM, Tucker WJ, Martin D, et al. Association of exercise and swimming goggles with modulation of cerebro-ocular hemodynamics and pressures in a model of spaceflight-associated neuro-ocular syndrome[J]. JAMA Ophthalmology, 2019, 137(6): 652-659. [68] Shinojima A, Kakeya I, Tada S. Lamina cribrosa pore diameter and spaceflight-associated neuro-ocular syndrome[J]. JAMA Ophthalmology, 2019, 137(11): 1330-1331. [69] Shen G, Link S, Tao Xiaofeng, et al. Modeling a potential sans countermeasure by experimental manipulation of the translaminar pressure difference in mice[J]. NPJ Microgravity, 2020, 6(1): 1-9. [70] Canac N, Jalaleddini K, Thorpe SG, et al. Review: pathophysiology of intracranial hypertension and noninvasive intracranial pressure monitoring[J]. Fluids and Barriers of the CNS, 2020, 17(1): 40. [71] Lerner DJ, Chima RS, Patel K, et al. Ultrasound guided lumbar puncture and remote guidance for potential in-flight evaluation of VIIP/SANS[J]. Aerospace Medicine and Human Performance, 2019, 90(1): 58-62. [72] 宫玉波, 吴斌, 罗灵, 等. 模拟长期微重力环境下大鼠眼底血流动力学,眼轴长度及血清中IFN-γ,IL-10含量的变化[J]. 眼科新进展, 2019, 39(9): 820-824. [73] 李向前, 任泽, 严伟明, 等. 长期微重力暴露所致眼损伤疾病动物模型的构建[J]. 实验动物科学, 2018, 35(03): 52-58. [74] 陈涛, 严伟明, 孙凯, 等. 尾部悬吊模拟微重力环境致大鼠眼部改变的研究[J]. 中华航空航天医学杂志, 2017, 28(2): 155-155. [75] Pandiarajan M, Hargens AR. Ground-based analogs for human spaceflight[J]. Frontiers in Physiology, 2020, 11: 716.
