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Divers can experience cognitive impairment due to inert gas narcosis (IGN) at depth. Brain-derived neurotrophic factor (BDNF) rules neuronal connectivity/metabolism to maintain cognitive function and protect tissues against oxidative stress (OxS). Dopamine and glutamate enhance BDNF bioavailability. Thus, we hypothesized that lower circulating BDNF levels (via lessened dopamine and/or glutamate release) underpin IGN in divers, while testing if BDNF loss is associated with increased OxS.
To mimic IGN, we administered a deep narcosis test via a dry dive test (DDT) at 48 msw in a multiplace hyperbaric chamber to six well-trained divers. We collected: (1) saliva samples before DDT (T0), 25 msw (descending, T1), 48 msw (depth, T2), 25 msw (ascending, T3), 10 min after decompression (T4) to dopamine and/or reactive oxygen species (ROS) levels; (2) blood and urine samples at T0 and T4 for OxS too. We administered cognitive tests at T0, T2, and re-evaluated the divers at T4.
Hyperbaric oxygen can have toxic effects on the central nervous system (CNS) (Gasier et al. 2017), but the mechanisms whereby narcosis induces cognitive impairment in divers are unclear. The present observational study reveals, for the first time, that, after a dry dive test at depth in a hyperbaric chamber to mimic in-depth sea diving, highly trained divers manifest: (1) cognitive impairment coupled to low circulating and/or saliva content of dopamine, glutamate, and BDNF; (2) overall increased ROS emission paralleled by depleted antioxidant levels; (3) pro-oxidizing and pro-inflammatory conditions likely subtending altered vascular reactivity; and (4) elevated neopterin and homocysteine levels that may account, on the one hand, for the onset of inflammation and loss of BDNF signaling, and thus cognitive deficits, on the other (Fig. 7).
Especially when recurrent, exposures to narcosis can desensitize GABAA receptors on dopamine cells and decrease glutamate release while increasing the sensitivity of NMDA receptors, resulting in overall neurological toxic effects and motor impairment (Rostain et al. 2016). Of relevance, deficits in cognitive performance in the underwater environment are significantly more frequent in anxious subjects (Hos et al. 2011). Notwithstanding, the reasons accounting for all the phenomena described above remain ill defined. This gap in our knowledge, the consequent lack of potential interventions directed to lower IGN incidence, and the eventual severity of its remote functional and psychological repercussions deserve more investigation. On the one hand, reaching this goal will allow divers to be more focused and efficient in completing the immersion. On the other, increased knowledge and awareness, along with possible chemical or pharmacological interventions directed to attenuate the effects of narcosis will reduce the extent of an athlete's anxiety while performing deep diving and the long-term consequences of recurrent narcosis episodes.
Hyperbaric hyperoxia with challenging variations in PO2 can develop inflammation and display augmented ROS production in mammals (Balestra et al. 2021; Bosco et al. 2018a, 2021; Morabito et al, 2011), leading to cell damage via oxidative modifications in proteins, lipids, and nucleic acids. Recently, we assessed ROS production in saliva samples by EPR spectroscopy to measure a 30-day saturation dive (Mrakic-Sposta et al. 2020). EPR is the only currently available technique capable of directly detecting oxygen-free radicals by specific spin probes (Dikalov et al. 2018). There are no studies investigating IGN-induced ROS during a dry dive test in the hyperbaric chamber using this very specific and quantitative methodology. This approach may help address a vexing question such as if the body of breath-hold or scuba divers actually emits more ROS (Mrakic-Sposta et al. 2019, 2020), what role it may have in IGN unfolding. Indeed, excessive ROS emission can impair synaptic plasticity and memory function (reviewed in Massad et al. 2011); on the other hand, ROS such as superoxide anion can directly quench NO., reducing its bioavailability, and thus the biological effects (Paolocci et al. 2001). Here, we show that a dry dive test boosts ROS emission and depletes total antioxidant capacity in otherwise healthy breath-hold divers, likely preparing the ground not only for a pro-oxidizing environment, but also for a pro-inflammatory terrain, as indicated by the rise in iNOS and homocysteine levels.
Of note, in our study the athletes breathed compressed air during descent and oxygen from 12 msw during decompression. When considering the narcosis mechanisms, it should be remarked that, in general, they are very similar to those of anesthetic gases, i.e., oxygen can dissolve in the fatty substances in the neuronal membranes and, because of its physical effect on altering ionic conductance through the membranes, it may reduce neuronal excitability. Surprisingly, however, a few studies made a vis-Ã -vis comparison between breathing air and enriched air nitrox (EAN) on IGN, and with controversial outcomes. Some highlighted worse psychomotor performance when using O2, EANx, or TRIMIX (Lafere et al. 2016, 2019; Balestra et al. 2018; Rocco et al. 2019). Conversely, others concluded that narcotic impairment was the same, although divers may perceive otherwise using TRIMIX (Piispanen et al. 2021).
Neopterin is a clinical marker of immune activation during inflammation, and it has been widely studied, particularly under stressful conditions (Gieseg et al. 2018). Moreover, high levels of this potent antioxidant could be generated by interferon-γ-activated macrophages and derive from the oxidation of 7,8-dihydroneopterin. Of note, neopterin levels are elevated in brain illnesses, such as depression (Celik et al. 2010; Maes et al. 2012). Intriguingly, when subjected to repetitive transcranial magnetic stimulation (rTMS), patients suffering from depression manifest symptom improvement, along with an inverse correlation between BDNF and neopterin. In fact, after rTMS, BDNF levels are more elevated and neopterin is lower than in sham-treated patients (Leblhuber et al. 2019). This evidence further supports the notion that a cross talk exists between BDNF and neopterin bioavailability that is central to IGN pathogenesis. At this time, we can only speculate that monitoring neopterin levels can serve as a footprint of narcosis duration/intensity.
Although nitrogen is chemically inert, its physical properties make it analogous to narcotic substances. The principal reason is its high solubility in lipoid matter [2]. The onset of symptoms of nitrogen narcosis varies from diver to diver. Mild signs and symptoms can appear at 30m, but some individuals might be susceptible at shallower depths.
Behnke et al. stated that nitrogen narcosis is not sufficient to be a problem at 30m, but the situation tends to be worse at deeper depths. Symptoms tend to develop in a subtle way, but with harmful effects, if ignored by the divers.
The final stage of nitrogen narcosis (ca. 100 msw) is more severe, and includes lethargy, drowsiness, and ultimately loss of consciousness. At these depths, however, when breathing air, the toxicity caused by the high partial pressure of oxygen would likely cause injury to the diver.
Highly trained and experienced divers gradually accommodate the narcotic effects of narcosis. They learn to tolerate more effectively the different stressors during deep dives and recognize their own signs and symptoms.
As mentioned above, individual physiological variability, as in alcohol, plays an important role [2], [4]. Usually, ascent at shallow depth will resolve the effects of nitrogen narcosis, reducing the symptoms of intoxication. However, a recent study by Balestra et al. showed that narcosis did not subside immediately after ascending to shallower depths, but its signs and symptoms remained even after the divers had surfaced [1].
The symptoms that appear below 100m are different from those observed in nitrogen narcosis, and they are called High Pressure Nervous Syndrome (HPNS). The occurrence of HPNS was first reported by Bennet during research in connection with nitrogen narcosis during submarine escape from British submarines. This condition includes behavioral symptoms and electrophysiological changes, such as tremors of the hands, myoclonia, increased reflexes, nausea and vomiting, dizziness, fatigue and somnolence (desire to sleep), and dyspnoea.
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Another interesting fact is that, aside from inert gases, it appears that we can also succumb to narcosis from high enough levels of that vital gas, oxygen. The reason is that too high a level of oxygen within the tissues can leave some of it metabolized, thus enabling oxygen to behave like an inert gas.
That year was also auspicious for yet another reason. On May 23, 1939, the U.S. Navy submarine, Squalus, suffered a catastrophic valve failure during a test dive off New Hampshire's Isle of Shoals. Fortunately it came to rest in just 240 feet of water, rather than the crushing depths just offshore. Only a quick salvage-and-rescue operation would save the lives aboard, but the depth made air diving operations less than ideal due to the effects of nitrogen narcosis. The situation provided the Navy with its first opportunity to try the then-experimental gas mixture heliox (helium-oxygen) to complete the rescue; and the Squalus salvage operation went down as one of the most famous and successful in U.S. Naval history. 041b061a72