Vascular Patterns in Iguanas and Other Squamates: Blood Vessels and Sites of Thermal Exchange

Squamates use the circulatory system to regulate body and head temperatures during both heating and cooling. The flexibility of this system, which possibly exceeds that of endotherms, offers a number of physiological mechanisms to gain or retain heat (e.g., increase peripheral blood flow and heart rate, cooling the head to prolong basking time for the body) as well as to shed heat (modulate peripheral blood flow, expose sites of thermal exchange). Squamates also have the ability to establish and maintain the same head-to-body temperature differential that birds, crocodilians, and mammals demonstrate, but without a discrete rete or other vascular physiological device. Squamates offer important anatomical and phylogenetic evidence for the inference of the blood vessels of dinosaurs and other extinct archosaurs in that they shed light on the basal diapsid condition. Given this basal positioning, squamates likewise inform and constrain the range of physiological thermoregulatory mechanisms that may have been found in Dinosauria. Unfortunately, the literature on squamate vascular anatomy is limited. Cephalic vascular anatomy of green iguanas (Iguana iguana) was investigated using a differential-contrast, dual-vascular injection (DCDVI) technique and high-resolution X-ray microcomputed tomography (μCT). Blood vessels were digitally segmented to create a surface representation of vascular pathways. Known sites of thermal exchange, consisting of the oral, nasal, and orbital regions, were given special attention due to their role in brain and cephalic thermoregulation. Blood vessels to and from sites of thermal exchange were investigated to detect conserved vascular patterns and to assess their ability to deliver cooled blood to the dural venous sinuses. Arteries within sites of thermal exchange were found to deliver blood directly and through collateral pathways. The venous drainage was found to have multiple pathways that could influence neurosensory tissue temperature, as well as pathways that would bypass neurosensory tissues. The orbital region houses a large venous sinus that receives cooled blood from the nasal region. Blood vessels from the nasal region and orbital sinus show anastomotic connections to the dural sinus system, allowing for the direct modulation of brain temperatures. The generality of the vascular patterns discovered in iguanas were assessed by firsthand comparison with other squamates taxa (e.g., via dissection and osteological study) as well as the literature. Similar to extant archosaurs, iguanas and other squamates have highly vascularized sites of thermal exchange that likely support physiological thermoregulation that “fine tunes” temperatures attained through behavioral thermoregulation.     

Extended lower trapezius island myocutaneous flap: a fasciomyocutaneous flap based on the dorsal scapular artery

The lower trapezius island myocutaneous flap is a useful flap in head and neck reconstruction. It is thin and pliable and can reach defects in most areas of the head and neck. Its usefulness in head and neck reconstruction has often been limited or discouraged by reports of significant failure rates. In this study, the vascular anatomy and clinical use of the extended lower trapezius myocutaneous flap based solely on the dorsal scapular artery system are elucidated, and experience gained performing 20 flaps over the past 5 years by using the extended lower trapezius myocutaneous flap is reported. The vascular anatomy of the dorsal scapular artery system is reviewed in 13 fresh cadaveric dissections by using methylene blue, latex injection studies, and radiologic examination.     

Arterio-venous heat exchange systems in the Jackass penguin Spheniscus demersus

Extensive arterio-venous associations occur in the head, axillae and legs of the Jackass penguin Spheniscus demersus. These vascular arrangements appear to facilitate counter-current heat exchange. The major heat exchange system in the head is the post orbital rete mirabile formed by the superior orbital artery. Blood from this rete supplies the eye, nasal passages and superficial jaw muscles. Other blood vessels supplying the superficial areas of the head and mouth associate closely with their corresponding veins.
In the axilla the brachial artery divides to form a humeral plexus of parallel running arteries each associating with up to three interlinking veins. Only the marginal vein does not associate with an artery. It appears that a shunt mechanism, which bypasses the veins in the humeral plexus, functions to permit heat loss when required; for instance in a heat-stressed bird breeding or moulting on land.
In both the upper and lower leg all the major arteries and their branches associate closely with corresponding veins.
The development of these arterio-venous associations indicates that Spheniscus demersus is adapted to a cool aquatic environment in which heat retention is of prime importance.     

Ontogenetic development of the ophthalmic rete in relation to brain cooling in chickens and pigeons

The brain cooling capacity of the altricial pigeon increases during posthatching growth at a higher rate than that of the precocial duck and chicken. To determine if this difference between the altricial and the precocial modes of development can be related to growth rates of the vascular heat exchanger involved in brain cooling (the ophthalmic rete), we performed a morphometric analysis of this structure during the post-hatching maturation of the three species. The number of vascular units in the rete did not change during development but differed significantly among species. The retia continued to grow in length and diameter in an exponential relation with body mass at similar rates in all species. The surface area of the retial arteries, which reflects the area available for countercurrent heat exchange, also increased exponentially with body mass, but without significant differences among the three species. However, the effectiveness of the rete in brain cooling, as indicated by the degree of brain cooling per unit of heat-exchange area in the rete, was higher in the altricial pigeon than in the precocial chicken and duck. It is concluded that the posthatching morphometric changes in the ophthalmic rete (rete ophthalmicum) are important for the development of brain cooling capacity, but cannot solely explain differences in brain cooling between growing altricial and precocial birds. These differences are most likely related to differences in the maturation of the central thermoregulatory control system and the peripheral effector mechanisms among the two groups of birds.     

Anatomy of the spinal accessory nerve plexus: relevance to head and neck cancer and atherosclerosis

The term spinal accessory nerve plexus may be defined as the spinal accessory nerve with all its intra- and extracranial connections to other nerves, principally cranial, cervical, and sympathetic. The term is not new. This review examines its applied anatomy in head and neck cancer and atherosclerosis. Over the centuries, general studies of neural and vascular anatomy and embryology formed a basis for the understanding upon which the plexus is described. During the past century, its anatomy and blood supply have come to be better understood. The importance of almost all of the plexus to head, neck, and upper extremity motor and sensory functions has come to be realized. Because of this understanding, surgical neck dissection has become progressively more conservative. This historical progression is traced. Even the most recent anatomic studies of the spinal accessory nerve plexus reveal configurations, new to many of us. They were probably known to classical anatomists, and not recorded in readily available literature, or not recorded at all. Human and comparative anatomic studies indicate that the composition of this plexus and its blood supply vary widely, even though within the same species their overall function is very nearly the same. Loss of any of these structures, then, may have very different consequences in different individuals. As a corollary to this statement, data are presented that the spinal accessory nerve itself need not be cut during surgical neck dissections for severe impairment to occur. In addition, data are presented supporting the theory that atherosclerosis by obstructing vessels to this plexus and its closely connected brachial plexus will very likely result in their ischemic dysfunction, often painful. Finally evidence, as well as theory, is stated concerning anatomic issues, methodology, outcome, and possible improvements in surgical procedures emphasizing conservatism.     

Anatomy of the veins of the head in the domestic fowl

The anatomy of the cephalic venous system in the fowl was studied in 19 specimens by means of latex-injected preparations and by dissection. The brain sinuses converge dorsally upon the large cervical sinus and vertebral veins. Dorso-ventral communication is provided by the occipital veins posteriorly, while the ophthalmic system unites both dorsal and ventral sinuses and the temporal rete with the extracranial veins anteriorly. The jugular veins are formed from the superficial branches of the facial veins and serve mainly as outlets for extracranial blood. They are united at the base of the head by a prominent transverse anastomosis which slopes caudally towards the larger, right jugular. As in mammals, the carotid veins envelop the internal carotid arteries and anteriorly form a bulbous sinus cavernosus around the inter-carotid anastomosis.     

The superior thyroid artery perforator flap: anatomical study and clinical series

The redundant tissues of the anterior neck are well suited as a donor site for fasciocutaneous flaps in head and neck reconstruction, with similar skin quality and numerous underlying perforators. However, historic cadaveric research has limited the use of this as a donor site for the design of long and/or large flaps for fear of vascular compromise. The authors undertook an anatomical study to identify the vascular basis for such flaps and have modified previous designs to offer the versatile and reliable superior thyroid artery perforator (STAP) flap. Forty-five consecutive computed tomographic angiograms of the neck were reviewed, assessing the vascular supply of the anterior skin of the neck. Based on these findings, eight consecutive patients underwent head and neck reconstruction using a flap based on the dominant perforator of the region. In all cases, a perforator larger than 0.5 mm was identified within a 2-cm radius of the midpoint of the sternocleidomastoid muscle at its anterior border. This perforator was seen to emerge through the investing layer of deep cervical fascia as a fasciocutaneous perforator and to perforate the platysma on its ipsilateral side of the neck, proximal to the midline. This was seen to be a superior thyroid artery perforator in 89 of 90 sides and an inferior thyroid artery perforator in one case. Eight consecutive patients underwent preoperative imaging and successful flap planning and execution based on this dominant perforator. The superior thyroid artery perforator (STAP) flap demonstrates reliable vascular anatomy and is well suited to reconstruction of a broad range of head and neck defects. CLINICAL QUESTION/LEVEL OF EVIDENCE: Therapeutic, IV.     

Posthatching development of the rete ophthalmicum in relation to brain temperature of mallard ducks (anas platyrhynchos)

In posthatching mallard ducks (Anas platyrhynchos), brain cooling improves with growth. To determine whether this may be correlated with growth-related changes in morphology of the rete ophthalmicum, we studied the development of this rete in immature mallards from hatching to 29 days of age. We found that the number of arteries and veins was fixed at hatching. The rete continued to grow, however, in length and vessel diameter during body and brain growth. The vascular surface area for heat exchange in the rete therefore also increased with body and brain mass. The increase in retial heat-exchange area was faster than the simultaneous increase in brain mass. The increase in body-to-brain temperature difference (delta T) described previously occurred nearly in direct proportion to heat-exchange area, such that the ratio of delta T to exchange area was nearly constant at about 0.1 degrees C per mm2 during growth. It is concluded that the increase in heat-exchange area of the rete ophthalmicum plays a major role in the development of brain cooling capacity of posthatching ducks.     

Guttural pouches, brain temperature and exercise in horses

Selective brain cooling (SBC) is defined as the lowering of brain temperature below arterial blood temperature. Artiodactyls employ a carotid rete, an anatomical heat exchanger, to cool arterial blood shortly before it enters the brain. The survival advantage of this anatomy traditionally is believed to be a protection of brain tissue from heat injury, especially during exercise. Perissodactyls such as horses do not possess a carotid rete, and it has been proposed that their guttural pouches serve the heat-exchange function of the carotid rete by cooling the blood that traverses them, thus protecting the brain from heat injury. We have tested this proposal by measuring brain and carotid artery temperature simultaneously in free-living horses. We found that despite evidence of cranial cooling, brain temperature increased by about 2.5 degrees C during exercise, and consistently exceeded carotid temperature by 0.2-0.5 degrees C. We conclude that cerebral blood flow removes heat from the brain by convection, but since SBC does not occur in horses, the guttural pouches are not surrogate carotid retes.     

Simple approach to harvest of the anterolateral thigh flap

The free anterolateral thigh flap has proven to be invaluable for many types of reconstruction, ranging from upper and lower extremity trauma to head and neck reconstruction. There exist some controversies relating to certain difficulties in flap harvest because of the intramuscular route of its major perforator, which can exceed 80 percent and create a longer, more tedious dissection. Strategies to expedite flap harvest and minimize technical challenges have been proposed. The authors propose a simplified approach to harvest the anterolateral thigh flap founded on topographic surface anatomy and the intrinsic vascular anatomy of the flap. No Doppler imaging or angiography is used for preoperative perforator mapping.     

Finite-element simulation of cooling of realistic 3-D human head and neck

Rapid cooling of the brain in the first minutes following the onset of cerebral ischemia is a potentially attractive preservation method. This computer modeling study was undertaken to examine brain-cooling profiles in response to various external cooling methods and protocols, in order to guide the development of cooling devices suitable for deployment on emergency medical vehicles. The criterion of successful cooling is taken to be the attainment of a 33 degrees C average brain temperature within 30 min of treatment. The transient cooling of an anatomically correct realistic 3-D head and neck with realistically varying local tissue properties was numerically simulated using the finite-element method (FEM). The simulations performed in this study consider ice packs applied to head and neck as well as using a head-cooling helmet. However, it was found that neither of these cooling approaches satisfies the 33 degrees C temperature within 30 min. This central conclusion of insubstantial cooling is supported by the modest enhancements reported in experimental investigations of externally applied cooling. The key problem is overcoming the protective effect of warm blood perfusion, which reaches the brain via the uncooled carotid arterial supply and effectively blocks the external cooling wave from advancing to the core of the brain. The results show that substantial cooling could be achieved in conjunction with neck cooling if the blood speed in the carotid artery is reduced from normal by a factor of 10. The results suggest that additional cooling means should be explored, such as cooling of other pertinent parts of the human anatomy.     

The angiosomes of the head and neck: anatomic study and clinical applications

The angiosome concept was introduced over a decade ago by Taylor and Palmer, whereby the body was considered to be composed anatomically of multiple three-dimensional composite blocks of tissue supplied by particular source arteries. Since then, detailed studies of the forearm and leg have been examined by Taylor and his coworkers. This study focuses on another region--the head and neck. Six fresh head and neck cadaver specimens were examined after infusion with a radio-opaque lead oxide mixture and correlated with over 24 previous body studies. The vascular anatomy of the skin, superficial musculoaponeurotic system (SMAS), muscles, brain, dura, and bone was examined. Each layer was painstakingly removed, photographed, labeled, and mapped to the respective arteries and veins. A radiologic subtraction technique was used to allow successive layers to be compared. This information was then scanned into a computer, analyzed, color coded, and labeled, thereby producing a three-dimensional study of the head and neck region to identify the respective angiosomes. As in previous detailed examinations of the leg and forearm, the angiosomes were found to be connected usually within tissues, such as muscle, skin, specialized organs or glands, rather than between the tissues. The muscles usually had vessels of two or more angiosomes supplying them and fell into three major groups based on the similarity of their arterial supply. In some areas, the midline anastomoses were rich, especially in the integument of the scalp, forehead, and lips. In other regions, the midline vascular connections were poor, especially in the tongue and palate. No fewer than 13 angiosomes of the head and neck, supplied by the branches of the external carotid, internal carotid, and subclavian arteries, have been defined, mapping their three-dimensional territories in the skin, the deep soft tissues, and the bones. Although most angiosomes spanned between skin and bone, three territories, those of the vertebral, lingual, and ascending pharyngeal vessels, were confined to the deep tissues without cutaneous representation. Finally, this study provides additional data for the surgeon to help plan safer incisions and better reconstructive flap procedures. It also gives information that may help explain the etiology and treatment of head and neck arteriovenous vascular malformations.     

Warm brain and eye temperatures in sharks

Temperatures in the brain and eyes of mako and porbeagle sharks (Lamnidae) are 5 degrees C warmer than the water while the brain and eye temperatures in six other species of pelagic sharks are within 0.1 degrees C of water temperature. An orbital rete mirabile is present in the porbeagle and mako sharks but absent in the cranial vasculature of eleven other species of pelagic sharks. The orbital rete in the head of the porbeagle and mako sharks acts as a heat exchanger which conserves metabolic heat and raises the local tissue temperatures. This brain and eye warming system should buffer the central nervous system from the effects of rapid temperature change. Warming of the retina may improve the visual sensitivity of these active predators.     

Brain thermal inertia,but no evidence for selective brain cooling,in free-ranging western grey kangaroos (<Emphasis Type="Italic">Macropus fuliginosus</Emphasis>)

Marsupials reportedly can implement selective brain cooling despite lacking a carotid rete. We measured brain (hypothalamic) and carotid arterial blood temperatures every 5 min for 5, 17, and 63 days in spring in three free-living western grey kangaroos. Body temperature was highest during the night, and decreased rapidly early in the morning, reaching a nadir at 10:00. The highest body temperatures recorded occurred sporadically in the afternoon, presumably associated with exercise. Hypothalamic temperature consistently exceeded arterial blood temperature, by an average 0.3°C, except during these afternoon events when hypothalamic temperature lagged behind, and was occasionally lower than, the simultaneous arterial blood temperature. The reversal in temperatures resulted from the thermal inertia of the brain; changes in the brain to arterial blood temperature difference were related to the rate of change of arterial blood temperature on both heating and cooling (P < 0.001 for all three kangaroos). We conclude that these data are not evidence for active selective brain cooling in kangaroos. The effect of thermal inertia on brain temperature is larger than might be expected in the grey kangaroo, a discrepancy that we speculate derives from the unique vascular anatomy of the marsupial brain.     

Structure and sympathetic innervation of the intracranial arteries in the giraffe (Giraffa camelopardalis)

Fluorescence histochemistry discloses that the carotid rete mirabile in the giraffe has a poor sympathetic innervation. In contrast, the efferent artery of the rete (internal carotid artery) and the cerebral arteries show moderate sympathetic innervation. A certain degree of regional variability was noted in which the rostral arteries (anterior and middle cerebral) receive more sympathetic nerves than the caudal (posterior communicating and basilar) arteries. The sympathetic nerves on the giraffe cerebral vessels may constitute part of a host of mechanisms by which regional blood flow to the brain is regulated. Conversely, the paucity of sympathetic innervation of the carotid rete mirabile may indicate that this structure does not play an active role in vasoconstrictor responses during postural changes of the head.     

Reconstruction of mandibular and floor of mouth defects using the trapezius osteomyocutaneous flap

The trapezius osteomyocutaneous island flap has evolved in postablative head and neck reconstruction as a versatile and hardy local flap which can provide intraoral lining, well-vascularized bone, and muscle bulk for the reconstruction of a complex defect. This investigative study examines the anatomy of 20 osteomyocutaneous flaps in 10 fresh cadavers and in 8 clinical patients. In our series, 80 percent (type I) of the major vascular pedicle arose from the thyrocervical trunk. In 20 percent (type II), the major pedicle arose separately from the subclavian artery. The regions perfused by the vascular trunk were further examined with microopaque and Prussian blue injections through the transverse cervical artery. Consistent areas of cutaneous staining as well as bony staining were noted over the shoulder, arm, and back and into the scapula itself. Experience with eight clinical applications of this osteomyocutaneous flap resulted in successful healing with an excellent aesthetic and functional result. Long-term follow-up was maintained on the patients for up to 36 months. Panorex radiographs and biopsies of the grafted bone were obtained on several patients. These disclosed evidence of bony remodeling and viable bone tissue. Tetracycline labeling also revealed evidence of active bony turnover.     

Orbital rete and red muscle vein anatomy indicate a high degree of endothermy in the brain and eye of the salmon shark

The salmon shark has been ranked as the most endothermic lamnid shark based upon geographical range, extent of slow twitch muscle, supra-hepatic rete size, and limited temperature measurements, yet its anatomy has remained largely undescribed, and measurements of brain or eye temperatures have not been reported. In this study, four specimens are examined to determine if the morphological requirements for warming the brain and eyes are present. A well-developed arterial orbital rete lies within a venous sinus on both sides of the cranium. Cool, oxygenated blood from the gills can pass through the vessels of this exchanger before reaching the brain or eyes. Since venous blood in the sinus flows opposite the arterial blood, counter-current heat exchange can occur. A vein originating in the red swimming muscle likely contributes to the warmth of the venous sinus by supplying blood directly from the warmest region of the shark. Before collecting in the orbital sinus, this red muscle vein bathes the brain in warm blood. These morphological data suggest the salmon shark has a significant capacity to warm the brain and eyes.     

Anatomy of the arteries of the head in the domestic fowl

The anatomy of the cephalic arterial system in the fowl was studied in 24 specimens by means of latex-injected preparations and by dissection. Branches of the external carotid artery supply the extracranial regions. The vertebral arteries unite with the occipitals and have no major communications with the encephalic system. Blood can reach the brain directly from the internal carotid artery and indirectly by way of the extensive cerebral-extracranial anastomoses; especially prominent are those to the palatine and sphenomaxillary arteries from the maxillary and facial branches of the external carotid artery. A large external ophthalmic artery supplies the temporal rete and eye musculature, and an internal ophthalmic artery links the rete and the cerebral vessels. The circle of Willis is incomplete both anteriorly and posteriorly; the anterior cerebral arteries do not unite and the basilar artery is generally asymmetrical in origin. The basilar artery tapers caudally and is continued as the ventral spinal artery.     

Limitations on arteriovenous cooling of the blood supply to the human brain

Arteriovenous heat transfer (AVHT) is a thermoregulatory phenomenon which enhances tolerance to thermal stress in a variety of animals. Several authors have speculated that human responses to thermal stress reflect AVHT in the head and neck, even though primates lack the specialized vascular arrangements which characterize AVHT in other animals. We modeled heat transfer based on the anatonmical relationships and blood flows for the carotid artery and associated venous channels in the human neck and cavernous sinus. Heat transfer rate was predicted using the effectiveness-number of transfer units method for heat exchanger analysis. Modeling showed that AVHT is critically dependent upon (1) heat exchanger effectiveness and (2) arteriovenous inlet temperature difference. Predicted heat exchanger effectiveness is less than 5.5% for the neck and 0.3% for the cavernous sinus. These very low values reflect both the small arteriovenous interface for heat exchange and the high flow rate in the carotid artery. In addition, humans lack the strong venous temperature depression required to drive heat exchange; both the cavernous sinus and the internal jugular vein carry a large proportion of venous blood warmed by its passage through the brain as well as a small contribution from the face and scalp, whose temperature varies with environmental conditions. Under the most optimistic set of assumptions, carotid artery temperature would be lowered by less than 0.1° C during its passage from the aorta to the base of the brain. Physiologically significant cooling of the blood supply to the brain cannot occur in the absence of a suitably scaled site specialized for heat exchange.