Location via proxy:   [ UP ]  
[Report a bug]   [Manage cookies]                
Next Article in Journal
Farm Animal Welfare Is a Field of Interest in China: A Bibliometric Analysis Based on CiteSpace
Next Article in Special Issue
Morphometric Analysis of Developmental Alterations in the Small Intestine of Goose
Previous Article in Journal
Detecting Forest Musk Deer Abscess Disease Pathogens Using 16S rRNA High-Throughput Sequencing Technology
Previous Article in Special Issue
Cocaine- and Amphetamine-Regulated Transcript (CART) Peptide Is Co-Expressed with Parvalbumin, Neuropeptide Y and Somatostatin in the Claustrum of the Chinchilla
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 13
Issue 19
10.3390/ani13193144
animals-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Communication

Arterial Blood Supply to the Cerebral Arterial Circle in the Selected Species of Carnivora Order from Poland

by
Maciej Zdun
1,2,
Jakub Jędrzej Ruszkowski
1,3,*,
Aleksander F. Butkiewicz
2 and
Maciej Gogulski
3,4
1
Department of Animal Anatomy, Poznan University of Life Sciences, Wojska Polskiego 71C, 60-625 Poznan, Poland
2
Department of Basic and Preclinical Sciences, Nicolaus Copernicus University in Torun, Lwowska 1, 87-100 Torun, Poland
3
University Centre for Veterinary Medicine, Szydłowska 43, 60-656 Poznan, Poland
4
Department of Preclinical Sciences and Infectious Diseases, Poznan University of Life Sciences, Wołynska 35, 60-637 Poznan, Poland
*
Author to whom correspondence should be addressed.
Animals 2023, 13(19), 3144; https://doi.org/10.3390/ani13193144
Submission received: 14 September 2023 / Revised: 30 September 2023 / Accepted: 6 October 2023 / Published: 8 October 2023
(This article belongs to the Special Issue Advances in Animal Anatomy Studies)
Browse Figures
Review Reports Versions Notes

Abstract

:

Simple Summary

Carnivores are a wide, diverse group of mammals whose representatives live all over the world. The study describes arterial blood supply to the cerebral arterial circle of the group of selected species in the Caniformia suborder living in Poland. The results were discussed based on the current knowledge of this field of research.

Abstract

Carnivores are a wide, diverse group of mammals whose representatives live all over the world. The study presents the results of the analysis of the arterial vascularization of the blood supply to the cerebral arterial circle of selected species in the Caniformia suborder living in Poland. The selected group consists of wild and farm animals—105 animals in total. Three different methods were used—latex preparation, corrosion cast, and cone-beam computed tomography angiography. The main source of blood for encephalon in the described species is the internal carotid artery, and the second one is the vertebral artery. The results were discussed in relation to the current knowledge of this field of research. Information on the potential physiological meaning of such vascular pattern has been provided.

1. Introduction

Carnivores (order Carnivora) are a diverse group of mammals that managed to populate many different habitats on all of the continents [1]. According to the International Union for the Conservation of Nature, there are 290 species belonging to this order [2]. The order consists of two suborders—Feliformia and Caniformia. In the study, only representatives of the Caniformia suborder were used. The described species belong to the Polish fauna and are members of four families—Canidae, Mustelidae, Procyonidae, Phocidae. Red fox (Vulpes vulpes), gray wolf (Canis lupus), European badger (Meles meles), Eurasian otter (Lutra lutra), and gray seal (Halichoerus grypus) are native to Polish fauna. The raccoon dog (Nyctereutes procyonoides), American mink (Mustela vison) and common raccoon (Procyon lotor) are invasive species. American mink is also a fur animal that is kept on farms.
The vascular patterns of arteries of different animal species have been the subject of anatomical research for decades. Various, often species-specific, vascular systems have been described in many species of carnivorous animals, often focusing on specific parts of the body. The cerebral arterial circle is among the most frequently described anatomical regions in this aspect [3,4,5]. The blood supply to these structures is often overlooked. The aim of this study was to assess and describe detailed arterial patterns of the arteries supplying blood to the arterial circle of the brain in the described species.

2. Materials and Methods

2.1. Animals

The study was conducted on 105 specimens of the Carnivora order of 8 species (Table 1). The animals used were adults of both sexes. Only animals without the trauma of the head and neck region were included in the research group. The animals were obtained from hunters, breeders, and zoos. All animals were obtained as post-mortem material. No animals were killed for the purpose of the study. The species distribution and number of individuals used in the study are presented in Table 1.

2.2. Methods

In the study, different anatomical methods were used to obtain a high-quality, complete image of the vascular pattern of the described area.
The classical anatomical preparation methods used in the study included latex preparation (method 1) and corrosion cast (method 2). A more advanced imaging method was the use of maximum-intensity projection reconstruction of cone-bean computed tomography scans (method 3). While working with the cadavers, additional precautions were taken. Researchers were wearing masks with high-quality filters and were working in a preparation room with an efficient ventilation system. The system settings were 20 air changes per 1 h.
Method 1
This method was used in 28 specimens. The method consists of injecting bilateral common carotid arteries with liquid, red LBS 3060 latex. After the injection, the preparations were cured in 5% formaldehyde solution for 14 days. The next step was rinsing specimens with running water for 48 h to flush out the excess formaldehyde. The next stage consisted of the manual dissection of soft tissues. The excess connective tissue was cut, which resulted in red arteries being obtained from the surrounding soft tissues.
Method 2
This method was used in 67 preparations. The method consists of injecting bilateral common carotid arteries with a tinged solution of the chemo-setting acrylic material Duracryl® Plus (SpofaDental, Jičín, Czech Republic). This material hardened after the injection, and the specimens were submerged in the detergent solution (Persil, Düsseldorf, Germany) for the process of maceration. The temperature of water used for this process was 42 °C. The process lasted 28 days. This method produced a red acrylic cast of the arterial vessels on the bone scaffold.
Method 3
This method was used in 10 preparations. The method consists of administering contrast agent (barium sulphate; barium sulphuricum 1.0 g/mL, Medana, Sieradz, Poland) to bilateral common carotid arteries. The scans were performed at the University Centre for Veterinary Medicine in Poznan, Poland, with the use of Animage Fidex computed tomography (Fidex Animage, Pleasanton, CA, USA).
After the examination, the scans were studied, and proper images were taken in FidexGUI (version 3.6.0, Animage, USA) with maximum-intensity projection image reconstruction.
The names of the anatomical structures were standardized according to Nomina Anatomia Veterinaria [6].
All of the photographs taken during the study were taken with a digital camera (Canon EOS 250D). The photographs were saved in JPG format. GIMP v2.10.18 digital image editing software was used to process the photographs.

3. Results

The main source of blood for encephalon is the internal carotid artery (arteria carotis interna). This artery branches off from the common carotid artery (arteria carotis communis) at the point where the main arterial stream becomes the external carotid artery (arteria carotis externa). The internal carotid artery at the initial segment creates a thickening called the carotid sinus (sinus caroticus) (Figure 1, Figure 2, Figure 3 and Figure 4). This is most demonstrable in the gray seal, next in the gray wolf and red fox, but in six red foxes, its expression is weaker. In the European badger, it is slightly embossed. In the raccoon dog and common raccoon, it is poorly marked and takes on a more elongated, less convex shape. In the American mink and Eurasian otter, this vessel branches off with the occipital artery (arteria occipitalis) via a common trunk. This trunk is short and there is no carotid sinus observed. No thickening is observed after the trunk has split into the internal carotid and occipital arteries.
Next, the internal carotid artery heads dorsorostrally and penetrates the carotid canal (canalis caroticus) through the caudal foramen of the carotid canal. In Canidae, this foramen is located near the caudal end of the tympanic bulla (bulla tympanica) (Figure 2 and Figure 5), in the Mustelidae (Figure 6) and common raccoon it is near to the middle of the length of the tympanic bulla, and in Eurasian otter (Figure 7 and Figure 8) it is positioned even more rostrally, in the one-third rostral part of the tympanic bulla. Thus, in this species of carnivores, the internal carotid artery enters the skull more rostrally, and the carotid canal is shorter.
The diameter of the extracranial segment of the internal carotid artery is larger than that of the occipital artery in foxes, European badgers, gray seal and American mink. In the raccoon dog, Eurasian otter and wolf, these vessels are of equal diameter. In the vascular variations, the diameter of the internal carotid artery is smaller than that of the occipital artery in one wolf, while in one Eurasian otter, the internal carotid artery is an artery with a larger lumen. The carotid canal runs along the medial surface of the eardrum. In the carotid canal, the vessel runs rostrally. At the level of the rostral foramen of the carotid canal, it forms a vascular loop, and changes direction by 180° (Figure 2 and Figure 5). For a short distance, it runs caudally. Then, it circles an arc once again, this time with a more gentle course, and heads dorsally, entering the cranial cavity. This vascular loop at the level of the rostral foramen of the carotid canal protrudes from the foramen in the gray wolf. This vessel protrudes slightly or is on the border of the foramen in the fox, raccoon dog and Eurasian otter; it does not protrude in the European badger. In the American mink, common raccoon and gray seal, this artery does not create a vascular loop. In the American mink via the rostral foramen of the carotid canal enters the branch from the ascendance pharyngeal artery (arteria pharyngea ascendens) and joins the internal carotid artery. In the fox, gray wolf, European badger and raccoon dog this branch from the ascendance pharyngeal artery joins the vascular loop (Figure 5). In other species, no connection was observed between the branch of the ascending pharyngeal artery and the internal carotid artery, although this vessel ran in close proximity to the aforementioned foramen. In the Eurasian otter, from the internal carotid artery branched off the small vessel that heads to the caudal wall of the pharynx. No ascending pharyngeal artery from the external carotid artery was observed. Before the internal carotid artery begins to form the cerebral arterial circle, it is joined by an anastomosing branch from the external ophthalmic artery (ramus anastomoticus) (Figure 9). The external ophthalmic artery is a branch from the maxillary artery (arteria maxillaris). This last vessel is a continuation of the external carotid artery. In the common raccoon, this connection is observed between the external ethmoid artery (arteria ethmoidalis externa) and the internal carotid artery. In two specimens, this connection is between the external ophthalmic artery and the internal carotid artery. No such connection was observed in the Eurasian otter, American mink and gray seal. The internal carotid artery then divides into the rostral cerebral artery (arteria cerebri rostralis) and the caudal communicating artery (arteria communicans caudalis). The latter is joined to the basilar artery (arteria basilaris).
The third source of blood is the vertebral artery (arteria vertebralis) (Figure 10). This vessel passes into the transverse process foramen (foramen processus transversus) of the cervical vertebrae.
Between the second and third cervical vertebra branches off the medial branch of the vertebral artery. Bilateral branches form the ventral spinal artery (arteria spinalis ventralis) (Figure 11). This artery heads cranially and joins the basilar artery. Moreover, the vertebral artery heads cranially and enters the transverse process foramen of the atlas. Then, it exits more cranially under the wing of the atlas. At that point, the anastomosing branch to the occipital artery (ramus anastomoticus cum a. occipitali) branches off. Such arterial connection was not observed in a seal. Next, the vertebral artery enters the lateral vertebral foramen (foramen vertebrale leterale) of the atlas, penetrates the vertebral foramen (foramen vertebrale) and joins the basilar artery. This pattern is present in the Eurasian otter, American mink, foxes and European badger. In the common raccoon, no ventral spinal artery joining the basilar artery was observed. In the gray seal, no anastomosing branch to the occipital artery was observed. Moreover, in this species, the ventral spinal artery branched off between the first and second cervical vertebra.

4. Discussion

The well-developed internal carotid artery is the main source of blood for the cerebral arterial circle in the dog [7,8,9], as well as the Arctic fox [7,10], common fox [11,12] silver fox [13], raccoon dog, and species of the seal family (Phocidae), mustelids family (Mustelidae), bear family (Ursidae), raccoon family (Procyonidae) [7] of the order Carnivora. In Feliformia, the second group of Carnivores, the extracranial part of the internal carotid artery is not present in adult animals [14,15]. In fetuses and young cats, this artery provides blood to the encephalon, but at about 4–8 weeks of age this artery is incomplete and the connection between the common carotid artery and the cerebral arterial circle ceases to function [15]. The connection of the cerebral arterial circle to the internal carotid artery has been found in some rodents (Rodentia): in the European beaver [16] and Canadian beaver [17], the Egyptian spiny mouse [18], the American muskrat [7], the rat [7,19] and the ursine [7]. A fully preserved internal carotid artery, which is the main source of blood to the brain, is found in all representatives of the odd-toed ungulates, i.e., the horse and other representatives of the family Equidae [7,20,21], in tapirs of the family Tapiridae and the rhinoceros of the family Rhinocerotidae [7]. It is also found in the rabbit and hare of the order Lagomorpha [7,22], in the Abyssinian highlander of the order Hyracoidea, in the wallaby and red kangaroo of the order Marsupialia, the two-toed sloth of the order Xenarthra, in the primates of the order Primates [7,23,24], and in the elephant of the order Proboscidea [25,26]. The different courses of this vessel in various animal species were described. In the horse, the course of the internal carotid artery is straight and it does not form a bend before entering the cranial cavity. This vessel runs on the dorsal and rostral surface of the medial compartment of the guttural pouch and passes through the ragged opening—foramen lacerum [27,28]. Then, it enters the cranial cavity, where it passes through the ventral petrosal sinus and enters the venous cavernous sinus; here, it forms an S-shaped curve [29,30]. Such a course also occurs in the donkey [31]. Similarly, in the dog, the artery takes a fairly direct course by way of the jugular foramen, through the occipito-tympanic fissure and into the cavernous sinus [32]. Thus, this vessel does not pass between the eardrum and scalene parts of the temporal bone, and thus does not interfere with sound perception, as pointed out by Zedenov [33]. A preserved internal carotid artery is also found in dolphins or narwhals. However, this vessel extends into the tympanic cavity, passing through the middle ear in a semicircular arc [34,35]. As is well known, for these marine mammals, their sense of hearing is their most important sense, and they use it to emit and receive infrasound. In light of this information, it can be assumed that the obliteration of this vessel in ruminants is not related to their emission of low-frequency sounds, but is merely the result of developmental changes associated with a change in the position of the eardrum portion of the temporal bone. To be sure, it would be necessary to compare the frequency range of the waves emitted by the vessel with the range of perceived sounds in these aquatic mammals, but Zedenov [33] does not specify such a range. In animals in which obliteration does not occur, the course of this vessel is different and the development of the cranial skeleton does not affect the course of the internal carotid artery. Strategies of vascularization of the encephalon are different. In some rodents, the basilar artery is the main source of blood. In the guinea pig, it directs as much as about 66% of the blood to the cerebral arterial circle [36]. A strong basilar artery has furthermore been described in the aguti [37], the porcupine [38], the capybara [39], the common degu [40], nutria [41], European ground squirrel [42], chinchilla [43] or red squirrel [44]. In camels, the basilar artery has a relatively large lumen; however, it does not supply this organ to such an extent [45]. In the dromedary, the internal carotid artery is responsible for supplying 13% of the blood to the rostral epidural rete mirabile [46], and the vessels emerging from the rete mirabile are primarily responsible for cerebral vascularization. In the dog, the internal carotid artery is also a strong vessel, accounting for half the diameter of the external carotid artery [32]. In ruminants, despite the obliteration of the internal carotid artery, the basilar artery does not contribute significantly to the blood supply to the brain, with the maxillary artery being of greatest importance [47,48,49]. In addition to the obvious role of this vessel in supplying blood to the brain, other roles of this vessel have also been considered. Maloney et al. [50] sought to test the hypothesis of the role of the internal carotid artery in selective cooling of the brain in the horse. This hypothesis relied on the exchange of heat between the blood in the vessel and the air sac with which it comes into contact. However, the authors themselves stated that, assuming that the contact between these structures is about 6% of the surface area of the bag, it is not possible for the air to flow through the air sac in such a way that the temperature of the blood in the vessel can be realistically reduced. The phenomenon of selective cooling of the brain has been described in ruminants. However, the rostral epidural rete mirabile is involved, along with the venous cavernous sinus, and the internal carotid artery is not involved. Cooler venous blood returning from the nasal cavity washes over the vessels of the weird network, causing a drop in the temperature of arterial blood flowing into the brain [51,52]. In addition, it is important to note a feature of this artery, which is the serpentine course of the intracranial portion of this vessel. Ruedi [53] equates the probable function of this fragment in the domestic horse to attenuate the pulse wave of arterial blood and protect the brain from a surge of pressure. This course of the vessel was also found in llama [54].

5. Conclusions

The results of this study describing blood supply to the arterial cerebral circle in selected species of Caniformia members from Poland enrich the status of the current knowledge in the field of the angiology of the Carnivora order. The results may also contribute as a baseline for further physiological and pathological studies in the field of veterinary medicine.

Author Contributions

Conceptualization, M.Z.; formal analysis, M.Z., J.J.R. and A.F.B.; resources, M.Z., J.J.R. and M.G.; writing—original draft preparation, M.Z., J.J.R. and A.F.B.; interpretation of data for the work: M.Z.; writing—review and editing, M.Z., J.J.R. and M.G.; figure preparation—J.J.R. and M.G.; supervision, M.Z. All authors have read and agreed to the published version of the manuscript.

Funding

The scientific activity was supported by grant 506.539.05.00 of the Young Researcher Program of the Faculty of Veterinary Medicine and Animal Science, Poznan University of Life Sciences, financed by the Polish Ministry of Science and Higher Education and statutory activity of Department of Basic and Preclinical Sciences, Nicolaus Copernicus University in Torun.

Institutional Review Board Statement

No approval of research ethics committees was required to accomplish the aims of this study because the experimental work was conducted only on cadavers. All procedures involving cadavers, in accordance with the law of 15 January 2015 for the protection of animals used for scientific or educational purposes, do not require the approval of the local ethics committee (Journal of Laws 2015, item 266).

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We would like to thank veterinary technician Szymon Stelting for his help with acquiring the CT scans.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Mittermeier, R.A.; Wilson, D.E. Handbook of the Mammals of the World: Vol. 1: Carnivores; Lynx Edicions: Barcelona, Spain, 2009; pp. 1–727. [Google Scholar]
  2. Fernández-Sepúlveda, J.; Martín, C.A. Conservation status of the world’s carnivorous mammals (order Carnivora). Mamm. Biol. 2022, 102, 1911–1925. [Google Scholar]
  3. Brudnicki, W. Brain Base Arteries: Pattern and Variation in the European Otter (Lutra Lutra). Anat. Histol. Embryol. 2012, 41, 358–361. [Google Scholar] [CrossRef] [PubMed]
  4. Depedrini, J.; Campos, R. A systematic study of the brain base arteries in the pampas fox Braz. J. Morphol. Sci. 2003, 20, 181–188. [Google Scholar]
  5. Ozudogru, Z.; Can, M.; Balkaya, H. Macro-anatomical investigation of the cerebral arterial circle (Circle of Willis) in red fox (Vulpes vulpes). J. Anim. Vet. Adv. 2012, 11, 2861–2864. [Google Scholar]
  6. International Committee on Veterinary Gross Anatomical Nomenclature. Nomina Anatomica Veterinária, 6th ed.; Editorial Committee: Hanover, Germany, 2017; pp. 73–147. [Google Scholar]
  7. Frąckowiak, H. Magistrale tętnicze głowy u niektorych rzedów ssaków [Arterial patterns of the head in selected mammalian orders]. In Roczniki Akademii Rolniczej w Poznaniu; Uniwersytet Przyrodniczy w Poznaniu: Poznań, Poland, 2003; pp. 5–80. [Google Scholar]
  8. Tanuma, K. A morphological study on the circle of Willis in the dog. Okajimas Folia Anat. Jap. 1981, 58, 155–175. [Google Scholar] [CrossRef]
  9. Wiland, C. Badania porównawcze gałęzi korowych tętnicy środkowej mózgu u niektórych gatunków drapieżnych (Carnivora). Zesz. Nauk. ATR Bydgoszcz. 1991, 44, 1–52. [Google Scholar]
  10. Wiland, C. Zakres zmienności układu tętnic podstawy mózgowia u piesaków. In Roczniki Wyższej Szkoły Rolniczej w Poznaniu; Dział Wydawnictw WSR: Poznań, Poland, 1967; Volume 10. [Google Scholar]
  11. Frąckowiak, H. Tętnice głowy u lisa pospolitego. In Roczniki Akademii Rolniczej w Poznaniu; Uniwersytet Przyrodniczy w Poznaniu: Poznań, Poland, 1978; Volume 101, pp. 59–66. [Google Scholar]
  12. Skoczylas, B.; Brudnicki, W.; Kirkiłło-Stacewicz, K.; Nowicki, W.; Wach, J. Cortical branches of the middle cerebral artery in silver fox (Vulpes vulpes). Pesqui. Veterinária Bras. 2016, 36, 1053–1057. [Google Scholar] [CrossRef]
  13. Frąckowiak, H.; Zawidzka, B. Tętnice głowy u lisa srebrzystego. Rocz. Akad. Rol. W Pozn. Zootech. 1990, 220, 27–36. [Google Scholar]
  14. Frąckowiak, H.; Godynicki, S. Brain basal arteries in various species of Felidae. Pol. J. Vet. Sci. 2003, 6, 195–200. [Google Scholar]
  15. Ziemak, H.; Frackowiak, H.; Zdun, M. Domestic cat’s internal carotid artery in ontogenesis. Vet. Med. 2021, 66, 292–297. [Google Scholar] [CrossRef]
  16. Frąckowiak, H.; Śmiełowski, J. Cephalic arteries in the european beaver Castor fiber. Acta Theriol. 1998, 43, 219–224. [Google Scholar] [CrossRef]
  17. Pilleri, G. Central nervous system, craniocerebral topography and cerebral hierarchy of the Canadian beaver (Castor canadensis). In Investigations on Beavers; Pilleri, G., Ed.; Institute of Brain Anatomy, University of Berne: Bern, Switzerland, 1983; Volume 1, pp. 19–59. [Google Scholar]
  18. Szczurkowski, A.; Kuchinka, J.; Nowak, E.; Kuder, T. Topography of arterial circle of the brain in Egyptian spiny mouse (Acomys cahirinus, Desmarest). Anat. Histol. Embryol. 2007, 36, 147–150. [Google Scholar] [CrossRef] [PubMed]
  19. Esteves, A.; Freitas, A.C.; Rossi-Junior, W.C.; Fernandes, G.J.M. Anatomical arrangement and distribution of the cerebral arterial circle in rats. J. Morphol. Sci. 2013, 30, 132–139. [Google Scholar]
  20. Zietzschmann, O. Die Arteria carotis interna des Pferdes und die Frage der Regulation ihrer pulsatorischen Schwankungen. Schw. Arch. Tierheilkd. 1922, 64, 509–515. [Google Scholar]
  21. Nickiel, R.; Schwarz, R. Vergleichende Betrachtung der Kopfarterien der Haussaugetiere (Katze, Hund, Schwein, Rind, Schaf, Ziege, Pferd). Comparative analysis of the head arteries of domestic mammals (cat, dog, pig, cattle, sheep, goat, horse). Zentralblatt Veterinärmedizin Reihe A 1963, 10, 89–120. (In German) [Google Scholar] [CrossRef]
  22. Godynicki, S. Tętnice głowy u zająca szaraka. Pol. Arch. Wet. 1976, 19, 101–114. [Google Scholar]
  23. Zdun, M.; Ruszkowski, J.J.; Gogulski, M.; Józefiak, A.; Hetman, M. Arterial Circle of the Brain of the Red-Necked Wallaby (Notamacropus rufogriseus). Animals 2022, 12, 2796. [Google Scholar] [CrossRef] [PubMed]
  24. Zdun, M.; Ruszkowski, J.J.; Gogulski, M. Cerebral Vascularization and the Remaining Area Supply of the Internal Carotid Artery Derivatives of the Red Kangaroo (Osphranter rufus). Animals 2023, 13, 2744. [Google Scholar] [PubMed]
  25. Watson, M. Contributions to the anatomy of the Indian elephant. Part IV. Muscel and blood vessels of the face and head. J. Anat. 1875, 9, 118–133. [Google Scholar]
  26. Mariappa, D. Anatomy and Histology of the Indian Elephant. In Circulatory System; Indira Pub. House: Michigan, IN, USA, 1986; pp. 129–146. [Google Scholar]
  27. Du Boulay, G.; Kendall, B.E.; Crockard, A.; Sage, M.; Belloni, G. The Autoregulatory Capability of Galen’s Rete Cerebri and Its Connections. Neuroradiology 1975, 9, 171–181. [Google Scholar] [CrossRef]
  28. Nanda, B. Blood supply to the brain. In Sisson and Grossman’s the Anatomy of the Domestic Animals; Getty, R., Ed.; Sounders Company: Philadelphia, PA, USA, 1975; Volume 1, pp. 973–1011. [Google Scholar]
  29. Colles, C.M.; Cook, W.R. Carotid and cerebral angiography in the horse. Vet. Rec. 1983, 113, 483–489. [Google Scholar] [CrossRef] [PubMed]
  30. MacDonald, D.; Fretz, P.; Baptiste, K.; Hamilton, D. Anatomic, Radiographic and Physiologic Comparisons of the Internal Carotid and Maxillary Artery in the Horse. Vet. J. 1999, 158, 182–189. [Google Scholar]
  31. Khairuddin, N.; Sullivan, M.; Pollock, P. Angiographic anatomy of the extracranial and intracranial portions of the internal carotid arteries in donkeys. Ir. Vet. J. 2017, 70, 12. [Google Scholar] [CrossRef] [PubMed]
  32. Gillilan, L. Extra- and intra-cranial blood supply to brains of dog and cat. Am. J. Anat. 1976, 146, 237–254. [Google Scholar] [CrossRef] [PubMed]
  33. Zedenov, W. Sosudistaja sistema Bovinae w sravnitelno-anatomiočeskom izučeni i voprosy specyfičnosti jeje morfołogii. IV. K voprosu obliteracji vnutrennoj sonnoj arterii u krupnogo rogatego skota. Arch. Anat. Gist. Embriol. 1937, 16, 490–508. [Google Scholar]
  34. Cozzi, B.; Huggenberger, S.; Oelschläger, H. Diving: Breathing, Respiration, and the Circulatory System. In Anatomy of Dolphins; Academic Press: London, UK, 2017; pp. 91–131. [Google Scholar]
  35. Vogl, A.W.; Fisher, H.D. The internal carotid artery does not directly supply the brain in the Monodontidae (Order Cetacea). J. Morphol. 1981, 170, 207–214. [Google Scholar] [CrossRef]
  36. Majewska-Michalska, E. The vertebrobasilar arterial system in guinea pig as compared with dog and human. Folia Morphol. 1998, 2, 121–131. [Google Scholar]
  37. Da Silva, R.S.B.; De Oliveira, G.B.; Oliveira, C.M.; Bezerra, F.V.F.; Câmara, F.V.; De Oliveira, R.E.M.; De Oliveira, M.F. Arterial vascularization of the brain of the agouti (Dasyprocta aguti Linnaeus, 1766). Semin. Ciências Agrárias 2016, 37, 773–784. [Google Scholar] [CrossRef]
  38. Aydın, A.; Yılmaz, S.; Dinç, G.; Özdemir, D.; Karan, M. The morphology of circulus arteriosus cerebri in the porcupine (Hystrix cristata). Vet. Med. 2005, 50, 131–135. [Google Scholar] [CrossRef]
  39. Reckziegel, S.H.; Lindemann, T. A systematic study of the brain base arteries in capybara (Hydrochoerus hydrochaeris). J. Morphol. Sci. 2017, 18, 103–110. [Google Scholar]
  40. Brudnicki, W.; Skoczylas, B.; Jabłoński, R.; Nowicki, W.; Brudnicki, A.; Kirkiłło-Stacewicz, K.; Wach, J. The arteries of the brain base in the degu (Octodon degus Molina 1782). Vet. Med. 2014, 7, 343–348. [Google Scholar] [CrossRef]
  41. Azambuja, R.; Goltz, L.; Campos, R. Systematization of the brain base arteries in nutria (Myocastor coypus). Acta Sci. Vet. 2018, 46, 1580. [Google Scholar] [CrossRef]
  42. Aydin, A.; Yilmaz, S.; Ozkan, Z.E.; Ilgun, R. The morphology of the circulus arteriosus cerebri in the ground squirrel (Spermophilus citellus). Vet. Med. 2009, 54, 537–542. [Google Scholar] [CrossRef]
  43. Kuchinka, J. Morphometry and variability of the brain arterial circle in chinchilla (Chinchilla laniger, Molina). Anat. Rec. 2017, 8, 1472–1480. [Google Scholar] [CrossRef] [PubMed]
  44. Aydin, A. The morphology of circulus arteriosus cerebri in the red squirrel (Sciurus vulgaris). Vet. Med. 2008, 53, 272–276. [Google Scholar] [CrossRef]
  45. Al Aiyan, A.; Menon, P.; AlDarwich, A.; Qablan, M.; Hammoud, M.; Shawaf, T.; Richardson, K. Vertebrobasilar contribution to cerebral arterial system of dromedary camels (Camelus dromedarius). Front. Vet. Sci. 2021, 8, 696707. [Google Scholar] [CrossRef]
  46. Ocal, M.; Erden, H.; Ogut, I.; Kara, M. A quantitative study on the retial arteries in one-humped camels. Ann. Anat. 1998, 180, 369–437. [Google Scholar] [CrossRef]
  47. Baldwin, B.A.; Bell, F.R. The contribution of the carotid and cerebral arteries to the blood pressure in sheep. J. Physiol. 1960, 151, 9–10. [Google Scholar]
  48. Baldwin, B.A.; Bell, F.R. Effect of clamping cartotid and vertebral arteries on the blood pressure in sheep. J. Physiol. 1960, 151, 39–40. [Google Scholar]
  49. Baldwin, B.A.; Bell, F.R. The anatomy of the cerebral circulation in the sheep and ox. J. Anat. 1963, 97, 203–215. [Google Scholar]
  50. Maloney, S.; Fuller, A.; Mitchell, G.; Mitchell, D. On the guttural pouch and selective brain cooling in equids. S. Afr. J. Sci. 2002, 98, 189–191. [Google Scholar]
  51. Hayward, J.N.; Baker, M.A. A comparative study of the role of the cerebral arterial blood in the regulation of brain temperature in five mammals. Brain Res. 1969, 16, 417–440. [Google Scholar] [CrossRef] [PubMed]
  52. Strauss, W.M.; Hetem, R.S.; Mitchell, D.; Maloney, S.K.; O′Brien, H.D.; Meyer, L.C.; Fuller, A. Body water conservation through selective brain cooling by the carotid rete: A physiological feature for surviving climate change? Conserv. Physiol. 2017, 5, cow078. [Google Scholar] [CrossRef]
  53. Ruedi, M. Topographie, Bau und Funktion der Arteria Carotis Interna des Pferdes; Gebr. Leemann & Co.: Zürich, Germany, 1922; pp. 1–39. [Google Scholar]
  54. Zdun, M.; Grzeczka, A.; Zawadzki, M.; Frąckowiak, H. The rostral epidural rete mirabile of the llama as a place of retrograde transport of various substances–anatomical basics. J. Cell Biol. 2021, 9, 105–109. [Google Scholar] [CrossRef]
Animals 13 03144 g001
Figure 1. Ventromedial view of the tympanic bulla region of the gray seal. Corrosion cast. The white bar corresponds to a length of 1 cm. bt—tympanic bulla; 1—common carotid artery; 2—carotid sinus; 3—internal carotid artery; 4—external carotid artery.
Figure 1. Ventromedial view of the tympanic bulla region of the gray seal. Corrosion cast. The white bar corresponds to a length of 1 cm. bt—tympanic bulla; 1—common carotid artery; 2—carotid sinus; 3—internal carotid artery; 4—external carotid artery.
Animals 13 03144 g001
Animals 13 03144 g002
Figure 2. Ventromedial view of the tympanic bulla region of the red fox. Medial part of the tympanic bulla has been removed. Corrosion cast. The white bar corresponds to a length of 1 cm. 1—common carotid artery; 2—carotid sinus; 3—initial part of the internal carotid artery; 4—the part of the carotid artery that penetrates the carotid canal; 5—the vascular look of the internal carotid artery near the rostral opening of the carotid canal.
Figure 2. Ventromedial view of the tympanic bulla region of the red fox. Medial part of the tympanic bulla has been removed. Corrosion cast. The white bar corresponds to a length of 1 cm. 1—common carotid artery; 2—carotid sinus; 3—initial part of the internal carotid artery; 4—the part of the carotid artery that penetrates the carotid canal; 5—the vascular look of the internal carotid artery near the rostral opening of the carotid canal.
Animals 13 03144 g002
Animals 13 03144 g003
Figure 3. Maximum intensity projection reconstruction of the angioCT scan of the head of the gray seal. The white bar corresponds to a length of 1 cm. 1—common carotid artery; 2—carotid sinus; 3—internal carotid artery.
Figure 3. Maximum intensity projection reconstruction of the angioCT scan of the head of the gray seal. The white bar corresponds to a length of 1 cm. 1—common carotid artery; 2—carotid sinus; 3—internal carotid artery.
Animals 13 03144 g003
Animals 13 03144 g004
Figure 4. Lateral view of branches of the common carotid artery of the gray seal. Latex preparation. The white bar corresponds to a length of 1 cm. 1—common carotid artery; 2—carotid sinus; 3—external carotid artery; 4—occipital artery; 5—internal carotid artery.
Figure 4. Lateral view of branches of the common carotid artery of the gray seal. Latex preparation. The white bar corresponds to a length of 1 cm. 1—common carotid artery; 2—carotid sinus; 3—external carotid artery; 4—occipital artery; 5—internal carotid artery.
Animals 13 03144 g004
Animals 13 03144 g005
Figure 5. Maximum intensity projection reconstruction of the angioCT scan of the head of the gray wolf. The white bar corresponds to a length of 1 cm. 1—common carotid artery; 2—internal carotid artery; 3—occipital artery; 4—ascending pharyngeal artery.
Figure 5. Maximum intensity projection reconstruction of the angioCT scan of the head of the gray wolf. The white bar corresponds to a length of 1 cm. 1—common carotid artery; 2—internal carotid artery; 3—occipital artery; 4—ascending pharyngeal artery.
Animals 13 03144 g005
Animals 13 03144 g006
Figure 6. Ventromedial view of the tympanic bulla region of the European badger. Corrosion cast. The white bar corresponds to a length of 1 cm. bt—tympanic bulla; 1—common carotid artery; 2—external carotid artery; 3—internal carotid artery.
Figure 6. Ventromedial view of the tympanic bulla region of the European badger. Corrosion cast. The white bar corresponds to a length of 1 cm. bt—tympanic bulla; 1—common carotid artery; 2—external carotid artery; 3—internal carotid artery.
Animals 13 03144 g006
Animals 13 03144 g007
Figure 7. Ventromedial view of the tympanic bulla region of the Eurasian otter. Corrosion cast. The white bar corresponds to a length of 1 cm. bt—tympanic bulla; 1—external carotid artery; 2—internal carotid artery.
Figure 7. Ventromedial view of the tympanic bulla region of the Eurasian otter. Corrosion cast. The white bar corresponds to a length of 1 cm. bt—tympanic bulla; 1—external carotid artery; 2—internal carotid artery.
Animals 13 03144 g007
Animals 13 03144 g008
Figure 8. Maximum intensity projection reconstruction of the angioCT scan of the head of the Eurasian otter. The white bar corresponds to a length of 1 cm. bt—tympanic bulla; 1—external carotid artery; 2—occipital artery; 3—internal carotid artery.
Figure 8. Maximum intensity projection reconstruction of the angioCT scan of the head of the Eurasian otter. The white bar corresponds to a length of 1 cm. bt—tympanic bulla; 1—external carotid artery; 2—occipital artery; 3—internal carotid artery.
Animals 13 03144 g008
Animals 13 03144 g009
Figure 9. Maximum-intensity projection reconstruction of the angioCT scan of the head of the European badger. The white bar corresponds to a length of 1 cm. 1—external carotid artery; 2—vertebral artery; 3—anastomosing branch to the occipital artery; 4—internal carotid artery; 5—external ophthalmic artery; 6—anastomosing branch from the external ophthalmic artery.
Figure 9. Maximum-intensity projection reconstruction of the angioCT scan of the head of the European badger. The white bar corresponds to a length of 1 cm. 1—external carotid artery; 2—vertebral artery; 3—anastomosing branch to the occipital artery; 4—internal carotid artery; 5—external ophthalmic artery; 6—anastomosing branch from the external ophthalmic artery.
Animals 13 03144 g009
Animals 13 03144 g010
Figure 10. Lateral view of the first three cervical vertebrae of the gray seal. Corrosion cast. The white bar corresponds to a length of 1 cm. C1—first cervical vertebra; C2—second cervical vertebra; 1—vertebral artery.
Figure 10. Lateral view of the first three cervical vertebrae of the gray seal. Corrosion cast. The white bar corresponds to a length of 1 cm. C1—first cervical vertebra; C2—second cervical vertebra; 1—vertebral artery.
Animals 13 03144 g010
Animals 13 03144 g011
Figure 11. Dorsal view of the arteries of the cervical spine of the American mink. Corrosion cast. The white bar corresponds to a length of 1 cm. 1—vertebral artery; 2—medial branch of the vertebral artery; 3—ventral spinal artery; 4—basilar artery; white circle—the place where vertebral artery wraps around the wing of the first cervical vertebra before entering the vertebral lateral foramen.
Figure 11. Dorsal view of the arteries of the cervical spine of the American mink. Corrosion cast. The white bar corresponds to a length of 1 cm. 1—vertebral artery; 2—medial branch of the vertebral artery; 3—ventral spinal artery; 4—basilar artery; white circle—the place where vertebral artery wraps around the wing of the first cervical vertebra before entering the vertebral lateral foramen.
Animals 13 03144 g011
Table 1. The number of specimens examined in this study.
Table 1. The number of specimens examined in this study.
FamilySpeciesMethod 1Method 2Method 3
CanidaeRaccoon dog (Nyctereutes procyonoides)510-
Red fox (Vulpes vulpes)5132
Gray wolf (Canis lupus)121
MustelidaeAmerican mink (Mustela vison)5132
European badger (Meles meles)5132
Eurasian otter (Lutra lutra)372
ProcyonidaeCommon raccoon (Procyon lotor)38-
PhocidaeGray seal (Halichoerus grypus)111
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Zdun, M.; Ruszkowski, J.J.; Butkiewicz, A.F.; Gogulski, M. Arterial Blood Supply to the Cerebral Arterial Circle in the Selected Species of Carnivora Order from Poland. Animals 2023, 13, 3144. https://doi.org/10.3390/ani13193144

AMA Style

Zdun M, Ruszkowski JJ, Butkiewicz AF, Gogulski M. Arterial Blood Supply to the Cerebral Arterial Circle in the Selected Species of Carnivora Order from Poland. Animals. 2023; 13(19):3144. https://doi.org/10.3390/ani13193144

Chicago/Turabian Style

Zdun, Maciej, Jakub Jędrzej Ruszkowski, Aleksander F. Butkiewicz, and Maciej Gogulski. 2023. "Arterial Blood Supply to the Cerebral Arterial Circle in the Selected Species of Carnivora Order from Poland" Animals 13, no. 19: 3144. https://doi.org/10.3390/ani13193144

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop