In this study, MOP of the ulna provided a good prediction of MAP in a hypovolemic model. This result differs from that of a previous study on African grey parrots that the MOP of ulnar and MAP were not correlated(5). The authors believe that improvements in the measurement techniques and protocols from previous experiences were the key points for this difference in findings (5). The major modifications made in this study include the use of a stylet to remove possible occlusions in and around the IO catheter and rechecking of the patency of IO catheter by aspiration instead of flushing, because studies have shown that IO needle clearance by flushing causes a prolonged drop in IO pressure (lasting approximately 8 min), whereas after clearance by aspiration, recovery is rapid (lasting 30 s) (11). In addition, significant differences have been reported in the median IO pressure as measured by different operators and those associated with different flushing times (12). Finally, our hypovolemic model allowed examination of the correlation between IO and AP under extreme blood pressures, which may amplify the originally obscured correlation under a normovolemic state.
The relationship between IOP and AP has been studied in humans, swine, rabbits, dogs, cats, mice, and African grey parrots (5, 9, 10). IOP is generally described as following the one-fourth rule, which means that MOP is one-fourth of MAP in mammals (9). Detailed values and relationships between IOP and AP are summarised in Table 1. In the tibia, the ratio of MOP to MAP ranged from 29.1–37.9% in the four stages, whereas in the ulna, the ratio was relatively wide, ranging from 52–75.3% in this study; the ratio in both IO sites was higher than that reported in most mammalian data (Table 1). In a similar study using the swine haemorrhage model, the MOP (of the humerus, tibia, and femur) to MAP ratio ranged from 20.1–26.3% (13). Birds differ from mammals in body mass because they have higher resistance in the arterial vessel walls, lower peripheral resistance, larger hearts, higher stroke volumes, and higher heart rates, which result in higher blood pressure values and allow sufficient cardiac output to meet their greater metabolic needs (14, 15); this might also account for the higher IOP percentage to AP. While the IOP values were closer to AP in birds, they could potentially be a better indicator of AP than that in mammals. In addition, in both IO sites, the ratio decreased following the severity of the hypovolemic state, which might explain the moderate to high simple linear correlation between MAP and MOP of the ulna in normovolemic, 20% and 30% blood loss status but not in 60% blood loss status.
The IOP value in pigeons in this study was comparable to that reported in other studies. The IOP value of the ulna was 57.33 ± 23.86 mmHg in the present data compared with 49.17 ± 29.94 mmHg reported in African grey parrots; the IOP value of the tibia was 30.45 ± 17.97 mmHg in the present data compared to 26.4 ± 13.0 mmHg reported in the tibia diaphysis of dogs, 16–36 mmHg in the tibia of rabbits, and 17.4 ± 8.2 mmHg in the proximal tibia of swine (5, 16–18) These results indicate that MOP of the ulna and tibia may not present large differences between species. Comparable results were obtained when the declining trend in both pressures in both groups was evaluated. The alternating trend of MOP of the ulna was fully correlated with that of AP, whereas this relationship did not exist in MOP of the tibiotarsus. A swine study revealed that the decline in humeral IOP was similar to that of AP, in which AP decreased by 19.3% and humeral IOP decreased by 17% per bleeding stage; however, the relationship was poorly demonstrated in IOP of the femur and tibia, which only decreased by 11.8% and 9.8% per bleeding stage, respectively (13). Therefore, IOP of the forelimbs seems to correlate better with systemic blood pressure than that of the hindlimbs in the hypovolemic model. Furthermore, a more consistent relationship was noted when the declining trend between IOP and AP was analysed, which indicates that IOP of the ulna can serve as an index of hypovolemia in avians.
Respiratory variations in both IOP and AP have been reported. In general, the IOP waveform is described as a positive and pulsatile wave affected by the blood pressure and respiratory phase (8, 9). In addition, in dogs and humans, respiratory variation is significantly obvious in mechanically ventilated and haemorrhage-induced hypotension patients (19, 20). In a swine hypovolemic model, with more amount of exsanguination, more obvious the variation occurred. However, the alternating pattern of the variability was not consistent between AP and IOP, as well as IOP from different IO sites (13). A similar pattern was noted in the current data, in that respiratory variation was more obvious in a more severe hypovolemic state, especially in the AP waveform. Because this phenomenon was more frequent in hypovolemic patients, respiratory variation serves as an index of hypovolemia in humans (21). In addition, due to the association with perfusion condition, respiratory variations can also serve as a parameter for monitoring the effect of fluid therapy (20). Nonetheless, in case of appropriate study designs and more evidence, the condition and its application in avian models need to be further investigated.
The generation of the incisura is closely related to the cardiac cycle. In addition to mammals and humans, owing to their relatively similar anatomical features and vascular trees, this feature is also observed in pulse waves in a wide range of avian species (22, 23). In the present study, the generation of the incisura persistently occurred in AP in every stage and was more prone to be noted in IOP of the ulna. Thus, when comparing the conditions in both IO sites, it may be rational to assume that IO circulation of the ulna is more closely related to systemic circulation than IO circulation of the tibiotarsus. This result also, to some degree, explains why IOP of the ulna demonstrated a better correlation with AP than with the tibiotarsus.
The hypovolemic model is based on the description of hypovolemic shock in birds, i.e. 20%, 25–30%, and 60% of blood loss corresponds to the complementary, early decompensatory, and decompensatory phases, respectively (24). In the first phase, blood pressure may be normal or increased; in the second phase, it may be normal or decreased; and in the third phase, it may be decreased (24). In the present data, the result of AP fully corresponded to that reported in the previous study. Furthermore, the same result was noted in MOP of the ulna but not in MOP of the tibiotarsus, which only demonstrated a significant difference between stages 1 and 4 and stages 2 and 4. These results indicate that the study designs were able to induce a series of satisfactory hypovolemic statuses, and again, MOP of the ulna was more closely related to AP than MOP of the tibiotarsus.
This study had two main limitations. First, there was a non-steady pressure value in the first 2–3 min after exsanguination, and determination of the steady pressure was subjective. Second, relevant research on this topic is lacking. Research on IOP and its association with AP in birds is still in its infancy, and the most relevant evidence is derived from mammals, making the discussion based mainly on current findings in mammals. In the future, insights into the physiologic and anatomic causes of the IO site, IOP and AP relation, value, and waveform features should be studied to investigate whether our findings can be reproduced in other avian species. In addition to the hypovolemic model, other conditions and variables, such as vessel occlusion, medication affecting blood pressure, disease, and muscle load, should be introduced to fully understand their effects on IOP.