Role of Flight Duration and Altitude in Ocular Health of Military Pilots

Introduction

Pilots in jet aircraft are frequently susceptible to the effects of accelerations and sudden drifting maneuvers in a way described as g-force. There are 3 components to this. Linear acceleration reflects a change of speed in a straight line, occurring during take-off or landing. Radial acceleration is the result of a change in direction, such as when a pilot performs a sharp turn, pushes over into a dive, or pulls out of a dive. Angular acceleration results from a simultaneous change in both speed and direction, which happens in spins and climbing turns [1].

Military pilots are prone to abrupt forces, including gravitational pull and variable barometric pressure. They often experience visual disturbances mid-air, typically starting with gradual constriction of peripheral eye fields at +2.5 or +3.0 G, depending on their hydration and fatigue level. With values getting closer to +4.0 G, they can start experiencing hemianopsia or even transient visual loss [2]. These events are usually entirely reversible thanks to the short duration of the ischemia, but is potentially harmful in the long run. One theory of glaucoma pathophysiology states that repetitive ischemia-reperfusion episodes are particularly harmful to neurons, leading to acceleration of the disease. Therefore, it seems important to analyze the quality of microvessels supplying the retina.

Other disorders in military aviation can result from a hypobaric environment with a lower oxygen concentration. Hypoxia in pilots is mostly due to the greater effort needed to pump blood back to the head during increasing g-force and consequent exertion. As a result, an event called GLOC (G-induced loss of consciousness) can occur [3]. Similar risk factors are observed in the pathology of altitude sickness, but they take place more gradually. Symptoms include headache, difficulty breathing and speaking, edema of the extremities, muscle spasms leading to limitation of movements, obscured vision, and hearing loss. This ailment mostly involves tourists, climbers, and workers who travel to places with a thinner atmosphere composition than where they usually reside. Prior physical training and gradual ascent with proper acclimatization help in adapting to unusual circumstances, thus mitigating the adverse effects. These symptoms usually arise from disturbed blood flow and poor oxygenation, which are modulated by changes in atmospheric pressure, leading to acute and chronic changes in the retina [4]. High-altitude retinopathy encompasses hemorrhages, cotton wool spots, enlargement and tortuosity of retinal vessels, papilledema, and macular edema, giving rise to symptoms such as blurred vision and scotomas [5]. First, blood vessels dilate to deliver more oxygen, leading to leaking and exudation, which then cause further disruptions, such as microaneurysms with capillary non-perfusion. Over time, this causes apoptosis of retinal cells, observed as atrophy of the GCC and RNFL layers. In this case, hypoxic stress occurs continuously through hours to days of exposure, in contrast to the situation of military pilots, for whom the abrupt perfusion changes are much shorter, enabling autoregulation mechanisms to compensate.

Anatomically, the retina has dual vasculature. The outer retina, comprised of photoreceptors with a very high oxygen consumption rate, mainly relies on choroidal perfusion. The inner retina, where ganglion cells reside, it supplied by the superficial and deep plexi, which are nets of multiple anastomoses originating from the central retinal artery. A drop in arterial oxygen partial pressure (PaO2) induces an immediate increase in retinal blood flow. However, the choroidal blood flow is less sensitive to lower PaO2, and increases only after a substantial drop in venous saturation. Choroid thickening was observed at >6000 m and stayed thicker after descent for a short period of time, whereas retinal thickening can occur at altitudes as low as 4500 m [6].

Choroidal thickness can increase with inflammation or stress-related diseases, called the pachychoroid spectrum. Notably, central serous chorioretinopathy is observed more often in pilots, although this matter is disputed. One can blame the stressful conditions of their work, but other researchers postulate a retinal pigment epitheliopathy is the main cause [7]. Pachychoroid has been observed in both high altitudes and at great depths, for instance in divers [8]. The parameters mentioned above can be measured non-invasively and with high precision through optical coherence tomography (OCT). Presently, the retina is the only part of the central nervous system (CNS) in which we can image both blood vessels and nerve fibers using non-invasive methods [9]. Therefore, this study evaluated the association between flight duration and altitude with retinal changes seen on OCT in 44 Polish military pilots.

Material and Methods

FORMAL ANALYSIS:

OCT uses near-infrared waves to visualize tissues through low-coherence interferometry, allowing a precise distinction of all retinal layers [10]. All scans were performed with RTVue-XR (Angiovue; Optovue, Inc., Fremont, CA, USA). Head stabilization was achieved by standard support of chin and forehead. Study participants were instructed to focus on the internal fixation target. Scans of low quality (<6), with artifacts, or blurred motion for which data were insufficient for proper analysis were excluded.

The GCC scan protocol consisted of 1 horizontal line with 7-mm scan length and 15 vertical lines with 7-mm scan length at 0.5-mm intervals centered at 1 mm temporally to the fovea. GCC thickness was measured as the distance between the internal limiting membrane (ILM) and the outer boundary of the inner plexiform layer (IPL), and was automatically calculated by the device (Figure 1). The RTVue-XR Avanti measures GCC thickness separately in the superior and inferior sector, as well as the average thickness in both sectors [11].

A cross-line scan was performed to obtain high-quality images of the retina and choroid. Subfoveal choroidal thickness (SCT) was measured manually, using a caliper in SD-OCT software. SCT was defined as the distance between the hyperreflective line corresponding to the outer boundary of the retinal pigment epithelium (RPE) and the hyperreflective line corresponding to the chorioscleral border. The measurements were obtained in the subfoveal region (Figure 2). Retinal thickness (RT), foveal thickness (FT), and parafoveal thickness (PFT) data were obtained from retinal maps using the same device. The data collected from both eyes of the studied patients were taken into analysis.

STATISTICAL ANALYSIS:

Numerical features were described using measures of central tendency (weighted arithmetic mean and median) and measures of dispersion (standard deviation, lower and upper quartile, and minimum and maximum value of the feature). Initially, the Shapiro-Wilk W test was performed to assess the normality of the distribution of the measurable feature and Levene’s test to assess the homogeneity of variance. A multivariate analysis of variance (ANOVA) without repetitions was performed to estimate the statistical significance of differences in the values of the measurements performed between the 2 groups of study participants, taking into account their age as a controlling variable. In the case of variables with a non-normal distribution, a generalized linear model with standard errors robust to deviations was used. In the above statistical models, intra-subject variability correction was used because the unit of study was 1 of the 2 eyes of the examined person. All study participants were assessed and measured in both eyes. To assess the strength, direction, and statistical significance of the correlation of selected measurable variables, the Spearman rank correlation coefficient P was calculated. A level of P<0.05 was considered statistically significant. All statistical calculations were performed using the Statistica™ package, version 14 (TIBCO Software, Inc., Palo Alto, CA, USA).

Results

GROUPS CHARACTERISTICS:

The pilots were flying either (1) supersonic fighter aircraft: F-16 (22 pilots, 50.00%) and MiG-29 (3 pilots, 6.82%); (2) helicopters: Mi-8 (6 pilots, 13.64%) and W-3 (10 pilots, 22.73%); (3) narrow-body airliners: Boeing 707 (1 pilot, 2.27%) and Boeing 737 (2 pilots, 2.27%); or (4) tactical airlifters: C-130 (1 pilot, 2.27%).

They were further split into 4 groups based on their total flight time: <1000 hours (7 pilots, 15.91%), 1000–2000 hours (17 pilots, 38.64%), 2000–3000 hours (14 pilots, 31.82%), and 3000–4000 hours (6 pilots, 13.64%).

Regarding their typical flight altitude, the pilots were grouped into 3 ranges: <5000 meters above sea level (6 pilots, 13.64%), 5000–10000 meters above sea level (13 pilots, 29.54%), and 10 000–20 000 meters above sea level (25 pilots, 56.82%).

GENERAL CHANGES IN MILITARY PILOTS:

Retinal thickness, foveal thickness, and parafoveal thickness did not differ significantly in the groups (P=0.5208, P=0.7490, P=0.6995, respectively) (Table 1). Similarly, there were no statistically significant differences in mean RNFL thickness and total GCC thickness between the study groups (P=0.1138, P=0.0721, respectively). There were no significant differences in choroidal thickness between the military pilots and the controls (P=0.4513).

CHANGES BASED ON TOTAL HOURS OF FLIGHT:

However, when pilots were split into groups based on their overall hours spent flying, a very significant correlation was revealed in reduction of subfoveal choroidal thickness (P=0.0010) proportionally to total flight time (Table 2). The GCC thickness and RNFL thickness seemed unchanged with longer flight experience, showing no statistically significant differences between the groups (P=0.8468, P=0.1135, respectively).

CHANGES BASED ON FLIGHT ALTITUDE:

Analyzing the above parameters in pilots depending on their flight altitude, SCT and RT were higher in these groups according to mean and median values, but the difference was not significant (P=0.4524, P=0.0527, respectively) (Table 3). On the contrary, the RNFL and GCC both show a relative depletion in pilots exceeding 5000 meters above sea level, but the difference was also not statistically significant (P=0.5950, P=0.2466, respectively). Nevertheless, the trends in these parameters are not consistent with higher altitudes of up to 20000 meters.

Discussion

The findings of this study suggest that military pilots experience some degree of vascular damage due to sudden changes in ocular perfusion in their demanding work environment. Posterior ciliary vessels supplying the choroid become progressively smaller in diameter upon reaching the RPE/Bruch’s membrane complex through Haller’s and Sattler’s layers, to alleviate the effect of too-high blood pressure reaching the sensitive retinal structures, which need adequate nutrients for visual processing. The SCT thinning indicates possible atrophic changes at the level of the choroid, while the retinal structures remain protected due to gradual compensation of systemic blood flow alterations by those several vascular layers.

A few case reports show that flying conditions can trigger retinal pigment epitheliopathy, causing apparition of central serous chorioretinopathy (CSCR). However, pilot and non-pilot patients did not differ significantly in terms of CSCR clinical data [12]. Airline pilots and cabin crew had thicker SCT, but there were no differences in the choroidal vascularity index (CVI) compared with healthy subjects [13]. CVI indicates the proportion of vessels in the total choroidal area, comprised of vascular and stromal components.

Retinal vessel density was reported to increase after rapid ascent and was inversely related to partial pressure of arterial oxygen [14]. A rapid ascent of a few thousand meters in <24 hours was associated with a significant increase in choroidal thickness [15], unrelated to acute mountain sickness, and reversible upon return to low altitude [16–18]. Increased vessel tortuosity after ascent has been documented, while retinal blood flow was significantly altered [19]. Compared to individuals steadily climbing to high altitudes, who experienced thickening of the retina along with the ganglion cells complex and retinal nerve fiber layer, we can deduce that mid-air dynamics do not allow for hyperemia due to blood flow deficit in g-force-related maneuvers; hence, atrophic changes are more prevalent. Elevated levels of oxidative stress can induce mitochondrial damage, inflammatory response, apoptosis, and structural and functional changes of the retina. These findings can explain why our group of pilots had such a vast span of choroidal measurements.

Acute exposure to high-altitude-related hypoxia does not exactly result in macular edema, but rather causes a slight increase in perimacular retinal thickness [20]. Fischer et al found that retinal thickness was increased except for a decrease in mean retinal thickness in the macula, correlating with acute mountain sickness symptoms [21]. Tian et al reported that following exposure to a high-altitude environment, the RNFL thickness increased in the temporal and nasal quadrants of the optic disc, while it decreased in the inferior quadrant. The RNFL also thickened in the upper and lower parts of the macular region, and the GCC became thicker in the upper macula. After returning to normal conditions, these measurements went back to their original levels, except the RNFL in the lower macula stayed thicker [22]. Our investigation did not reveal a statistically significant difference between GCC thickness in military pilots compared to controls, but a greater GCC loss in the lower hemisphere was noticed, which is related to blood condensation in this area with gravitational force, leading to cell injury through overperfusion. Of note, the impact in anterior ischemic optic neuropathy is greater in the upper hemisphere, supposedly due to gravity pulling blood towards lower quadrants of the retina, leaving an inadequate supply for neurons located above the optic disc [23].

A similar study using OCT-A (OCT angiography)was performed to assess the retinal microvascularity in military pilots [24]. These pilots of high-performance fighter jets experience more measurable differences in retinal vessel parameters (diameter, density, tortuosity) compared to those flying transport aircrafts due to the different cockpit environment, hypobaric conditions, and g-force exposure. High-altitude exposure appears to cause decreased vessel density, particularly in the deep capillary plexus, which might result from ischemic events or atrophic retinal alterations due to unstable blood flow. Enlargement of the foveal avascular zone (FAZ) area, associated with longer flight times, further indicates ischemic effects resembling those seen in diabetic retinopathy. These findings could contribute to understanding how extreme environments and operational demands impact microcirculation, and this could also translate, for example, to inner ear changes), which is especially relevant given the trend toward increased space travel.

The main limitation of the current study is its relatively small number of the participants. With more participants, some of the differences in parameters between groups could gain statistical significance. Military pilots are required to meet rigorous health standards; therefore, their overall good health might be the reason for the relative stability of retinal and choroidal parameters due to having strong autoregulation mechanisms. Another limitation results from using a single-device method of assessment, and more insight could be gained from performing multi-modal imaging, including Doppler ultrasound imaging of the ophthalmic artery and central retinal artery, as well as electrophysiological exams.

Conclusions

The results of our study suggest that retinal thickness, GCC, and RNFL parameters remain stable in professional military pilots despite repetitive disturbances in ocular perfusion. However, these working conditions were observed to cause decreased subfoveal choroidal thickness. Longitudinal observation of the pilots group and study in a larger cohort would be advised to obtain more conclusive results and strengthen the implications for aviation professionals.