This study monitored vascular parameters of retinal blood vessels across NFLVP, SVP, SVC, ICP, DCP, DVC, as well as CC and large and medium choroidal blood vessels revealing that uncomplicated phacoemulsification significantly improved macular hemodynamics. We consider these changes to be favorable and beneficial.
Major results
A significant increase in VA, VPA, TNJ, JD, TVL and AVL was found, followed by the decrease in TNEP and ML manifesting rise in blood supply of the central macula after phacoemulsification (Additional file 1: Table S3; Table S4). Most changes in vascular parameters were evident one week after surgery and remained stable up to three months after surgery. These changes affected all retinal layers but not CC and choroid (Additional file 1: Table S5; Table S6). Observed patterns of alterations between the retina and choroid were somewhat expected as these two layers have different hemodynamic properties.
Functional hyperemia
Inflammatory response after uncomplicated phacoemulsification is imputed to be the cause of increased macular thickness, reaching its maximum between one week and one month after surgery and returning to baseline after 2-6 months [2, 15, 16]. However, none of these studies actually measured the local release of inflammatory metabolites. On the contrary, the prevailing view modelled from our study results' was that increase in macular hemodynamics could not be the result of postoperative inflammation as the changes persisted three months after the surgery, when inflammatory response should have been over [2, 15, 17-19], nor decrease in IOP due to OPP consistency (Additional file 1: Table S2) [3]. Moreover, all patients underwent uncomplicated phacoemulsification with favorable, low PHACO time and CDE (Additional file 1: Table S1), while factors contributing to neural damage and blood-brain barrier breakdown were excluded prior to enrolment.
Thus, the third mechanism, functional hyperemia, disclosed that blood flow in retinal vasculature significantly varied due to increased intensity of light stimulus after cataract removal, in stark contrast to choroidal circulation [5]. Namely, cataract blocks up to 40% of light at different wavelengths [20]. Increase in metabolism which accompanies neuronal activity lowers O2 and glucose levels and leads to production of vasoactive metabolites [21]. Products of neuronal activity adenosine, lactate and arachnoidic acid cause vasodilatation and functional hyperemia to compensate for energy consumption and increase in ganglion cell activity due to light stimulation restoring O2 and glucose levels [5, 22, 23]. Likewise, larger blood flow is induced after a period of dark adaptation [23], what in our case, hypothetically, we could consider cataract to be as cataracts gradually weaken the intensity of light stimuli.
SVC vs DVC
The greatest increase in VA, VPA, TNJ, JD, TVL and AVL was found in SVC (Additional file 1: Table S4). Due to functional hyperemia, AVL increased more than TVL suggesting coiling of blood vessels (Additional file 1: Table S4).
On the contrary, the greatest change of ML as an index for vascular structural non-uniformity, [12] appeared in DVC (Additional file 1: Table S4). These differences suggest different metabolic demands of retinal layers supplied by SVC and DVC.
NFLVP, a layer of long capillaries with small number of anastomosis located only in the posterior pole [6, 24], is presented with unique configuration (Additional file 1: Table S7) manifesting the highest number of end points and the lowest number of junctions (Table 2; Additional file 1: Table S7; Table S9).
Three months after surgery VA, VPA, TNJ, JD, TVL and AVL were significantly higher in DVC compared to SVC, while TNEP and ML were significantly higher in SVC (Additional file 1: Table S10). On the contrary, while comparing SVP and DCP (Additional file 1: Table S8), greater VA and VPA for SVP network were found likewise [10], but DCP showed higher TNJ, JD and TVL. Aforesaid attributes could correlate to the larger diameter of the SVP vasculature opposed to DVP being solely capillary meshwork [25]. Morphometry of ICP and DCP did not demonstrate significant differences (Additional file 1: Table S8).
Until this date, only two OCT-A studies analyzed retinal blood vessels after uncomplicated phacoemulsification [2, 3]. Performed on a relatively small subject samples (N = 9 and N = 32), they used different OCT-A devices while Q and EA comparison before and after cataract surgery was not performed [2, 3]. Zhao et al observed parafoveal and perifoveal blood vessels density increase one week after phacoemulsification lasting up to three months after surgery [3]. Furthermore, cataract surgery was followed by a decrease in the foveal avascular zone surface, and an increase in full and inner retinal thickness, occurring one week after surgery, and still increasing up to three months after the surgery [3]. Outer retinal thickness remained almost unchanged [3]. The vascular pattern responses observed here could give the anatomical background for the aforementioned results. Although all retinal layers demonstrated increase in perfusion, SVC underwent greater change than DVC (Additional file 1: Table S4). Inner plexiform layer contains both superficial and deep blood vessels [6]. Thus, the functional hyperemia observed could cause an increase in full and inner retinal thickness [3]. On the contrary, we hypothesize that functional hyperemia identified in DCP cannot elicit significant changes of outer retinal thickness as DCP is intersected between INL and OPL [6], justifying Zhao’s et al results [3].
Choroid
CC presented with the greatest VA, VPA, TNJ, JD, TVL and AVL, and the lowest TNEP and ML (Additional file 1: Tables S5; Table S9) confirming its structure as a continuous capillary meshwork with a high number of anastomosis [25]. Opposed to the retina, we found no significant changes in the choroid (Additional file 1: Table S6) and CC (Additional file 1: Table S5), except for TNEP and ML in CC. Light stimulation has a little effect on choroidal circulation, insensitive to pO2 fluctuations [5]. We thus concluded that physiological requirements outlined with low PHACO time and CDE did not reach the threshold to induce outer blood-retinal barrier breakdown and inflammatory response. Further, significant decrease of TNEP and ML in CC (Additional file 1: Table S5) could result from increased demand in heat dissipation through opening of anastomoses corroborating with published studies [2, 16, 26]. Some authors hypothesized increase in subfoveal thickness to be a consequence of local choroidal inflammatory response but found no reasoning for these changes, while correlation to CDE was not reported [18, 25, 27].
Ageing
Ageing causes altered hemodynamics and hypoperfusion mostly in neural tissues with high metabolic demand [28]. Decline in metabolic activity under physiological ageing was further supported by our study correspondingly, as retinal macular perfusion significantly increased after uncomplicated phacoemulsification and augmented visual stimulation.
Image quality
One might ask if these changes in macular perfusion after surgery were the result of better image quality after cataract removal. Thus, we counterbalanced this potential bias. OCT-A may overcome early stage cataract in contrast to clinically significant ones [29]. As follows, this study included only patients with mild to moderate opacities, graded objectively (Table S1). Secondly and more important, OCT-A image quality (Q) quantified by the software integrated in HRA+OCT Spectralis® before and after surgery was statistically the same (Table 1). Consequently, perfusion changes demonstrated here were unlikely the result of the improvement of the ocular optics after cataract removal. Furthermore, different time frames of perfusion alterations were demonstrated (Tables 2-8; Additional file 1: Table S5). In addition, the latest software version of Spectralis® uses the Position Artefact Removal tool, eliminating blood movement artefacts and enabling even more distinct analysis of deeper layers [9]. With TruTrack Active Eye Tracking technology high-quality retinal imaging even with eye movements is allowed [9].
There are few limitations to this analysis. First, we reported the values for only 55 subjects of Caucasian descent for whom we did not measure retinal metabolic activity. Further studies using OCT-A are needed to establish a normative database of observed vascular parameters for other demographic variables. Second, the analysis of retinal and choroidal pathology was beyond the scope of this report.