The Posterior Displacement of the Bruch's Membrane Opening: A Surprising Finding in Spaceflight-Associated Neuro-Ocular Syndrome

We read with great interest the article by Sibony et al.¹ entitled “Ocular Deformations in Spaceflight-Associated Neuro-Ocular Syndrome and Idiopathic Intracranial Hypertension” published recently in Investigative Ophthalmology & Visual Science. We would like to congratulate the authors for their commendable work in comparing changes in peripapillary shape of Bruch's membrane layer and displacements of Bruch's membrane opening (BMO) in crewmembers on long-duration spaceflights to patients with papilledema caused by idiopathic intracranial hypertension (IIH). Their study showed substantial differences in the degree of optic disc edema and the magnitude and pattern of ocular deformations between IIH and spaceflight-associated neuro-ocular syndrome (SANS), suggesting that there may be fundamental differences in the underlying biomechanics.¹ We would appreciate the opportunity to comment on the authors’ discussion of the possible reasons for the observed posterior BMO-displacements in crewmembers with SANS. 

Sibony et al.¹ found that in patients with IIH with papilledema, the BMO was preponderantly (in 80% of the eyes) displaced anteriorly (positive, toward the vitreous) whereas BMO displacements among eyes of crewmembers with SANS were bidirectional (48% displaced posteriorly, 36% displaced anteriorly, and 16% “nil”). Given that a rise in orbital cerebrospinal fluid pressure is assumed to occur in microgravity because of mildly elevated intracranial pressure or compartmentation of cerebrospinal fluid in the orbital subarachnoid space,^2,3 the posterior BMO displacement observed in most crewmembers with SANS is very surprising. As noted by the authors, the peripapillary indentation load (caused by choroidal expansion or orbital tissue pressure), interstitial prelaminar optic disc edema, changes in the compliance of the load-bearing structures, and the unequal displacement of the reference points and the BMO acting in part or together could potentially explain the “posterior” ocular deformations in SANS.¹ We fully agree that BMO displacement in SANS is likely multifactorial and, more specifically, that spaceflight-induced fluid accumulation in the prelaminar optic nerve head could potentially favor posterior BMO displacement away from the vitreous. We recently hypothesized that long-duration spaceflight may result in prelaminar fluid accumulation because of vascular leakage, as well as decreased interstitial fluid outflow through the ocular glymphatic system.^4–6 We further proposed that such prelaminar interstitial fluid accumulation might displace the BMO posteriorly and that this could be a contributing factor to the posterior BMO displacement observed in crewmembers with SANS.⁶ The study by Sibony et al.¹ seems to support this possibility. If prelaminar interstitial fluid contributes to the observed posterior displacement of the BMO in SANS, then eyes with greater increases in total retinal thickness (TRT) would be expected to demonstrate posterior BMO displacements. The authors found a statistically significant relationship between change in TRT, quantified within an elliptical annular region 250 µm from the BMO, and BMO displacement (P = 0.01).¹ As shown in their Supplementary Figure S2i, the authors demonstrated that crewmembers with the greatest increases in TRT had the greatest posterior BMO displacements.¹ Furthermore, it appeared that differences in deformations between IIH and SANS could not be entirely explained by the inequality in the degree of optic disc edema alone.¹ Indeed, reducing the disparity in swelling by comparing a subgroup of IIH with “mild papilledema” to crewmembers with large increases in TRT (“advanced SANS”) did not alter the basic patterns of ocular deformations in either cohort.¹ We believe that one possible explanation could be that in IIH, a prominent translaminar pressure gradient favoring intracranial pressure over intraocular pressure could overshadow any possible opposite effect of optic disc edema. 

Obviously, further research is needed to provide additional insight regarding the relative contribution of prelaminar interstitial fluid accumulation to the posterior BMO displacement observed in crewmembers with SANS. Continued analysis of the load-bearing structures of the optic nerve head by optical coherence tomography imaging in International Space Station crewmembers, and follow-up post-flight studies could provide important structural information in this respect and could lead to a better understanding of the pathogenesis of optic disc edema in astronauts. We therefore wish to encourage further research in this area. 

Acknowledgments

Disclosure: P. Wostyn, None; C.R. Gibson, None; T.H. Mader, None