Morphologie (2018) 102, 61—68

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HISTORY OF MORPHOLOGY

A critical appraisal of 11th century treatiseby Ibn Sina (Avicenna) on the anatomy ofthe vascular system: Comparison withmodern anatomic descriptionsUne évaluation critique du traité du xie siècle par Ibn Sina(Avicenne) sur l’anatomie du système vasculaire :comparaison avec les descriptions anatomiques modernes

P. Mazengenyaa,∗, R. Bhikhaa,b

a School of Anatomical Sciences, The University of the Witwatersrand, Faculty of Health Sciences, 7, YorkRoad, Parktown, Johannesburg, South Africab Ibn Sina Institute of Tibb, 1137 Anvil Road, Robertsville, Roodepoort, Johannesburg, South Africa

Available online 18 May 2018

KEYWORDSAvicenna;Vascular system;Arteries;Veins;Heart;Circulation

Summary Ibn Sina (also known as Avicenna in the West) was the most famous physician andmedical scientist of the medieval era. His book, the Canon of Medicine comprised a vast collec-tion of medical information ranging from basic medical sciences to specialised medical fields.Herein, we present an analysis of the cardiovascular system, particularly giving an in-depthcomparison of the structural and functional anatomy of the arteries and veins of the bodyas described by Avicenna in the Canon of Medicine and comparing them to modern extantanatomical literature.© 2018 Elsevier Masson SAS. All rights reserved.

Résumé Ibn Sina (également connu sous le nom d’Avicenne en Occident) était le plus célèbremédecin et scientifique médical de l’époque médiévale. Son livre, le Canon de la Médecine(littéralement le Livre des lois médicales), comprenait une vaste collection d’informationsmédicales allant des sciences médicales de base aux domaines médicaux spécialisés. Ici, nous

présentons une analyse du système cardiovasculaire, en examinant et comparant minutieuse-ment en particulier et en profondeur, l’anatomie structurelle et fonctionnelle des artères etdes veines du corps, telles qu’elles sont décrites par Avicenne dans le Canon de Médecine, eten les comparant aux vaisseaux présentés dans à la littérature anatomique existante.© 2018 Elsevier Masson SAS. Tous droits reserves.

∗ Corresponding author.E-mail address: pedzisai.mazengenya@wits.ac.za (P. Mazengenya).

https://doi.org/10.1016/j.morpho.2018.03.0011286-0115/© 2018 Elsevier Masson SAS. All rights reserved.

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he circulatory system and its underlying mechanismemained a mystery until the 7th century AD. [1]. Severalheories were described in relation to the heart and vesselslthough there was no clear understanding of their cardio-ascular functions. Circulation of blood was first mentionedn ancient Chinese literature as part of their traditionaledicine but was not associated with the pumping action

f the heart; instead it was caused by the opposing forcesf Yin and Yang [1]. In agreement with Aristotle and thencient Indians, Avicenna regarded the heart as source ofhe nervous system, emotions and control mechanism of theest of the body [1,2]. Hippocrates (460—370 B.-C.) thoughthat the liver and the spleen were responsible for the pro-uction of blood which will then travel to the heart to bearmed and or cooled by air from the lungs (Fig. 1) [1,3,4].tructurally, Aristotle (384—322 B.-C.) described the threehambered heart and noticed that blood filled with breatheave the heart through a large vessel called the aorta [1].

Functionally the earlier concepts about circulation wereased on the refinement of ingested food in the liver to pro-uce blood that will be distributed by the veins throughouthe body and be assimilated and incorporated into flesh [4].enous blood, in addition to nutrition also contained otherumours, including yellow and black bile [4]. In ancientreek medicine Unani (Tibb), the humoral theory is basedn the hypothesis that each individual has an ideal humoralalance which is made up from the four humours namelylood (sanguinous), phlegm (serous), yellow bile (bilious),lack bile (melancholic) [5]. According to Unani (Tibb) phi-osophy as long as the ideal humoral balance of an individuals maintained, health (homeostasis) will prevail [6,7].

In modern medicine the concepts of blood circulation putorward by William Harvey (1578—1657 AD) are regarded as

turning point, however a lot of information has been disre-arded prior to Harvey. In addition as Harvey stated ‘‘theres no science which does not spring from pre-existing knowl-dge’’ [4]. Thus in this article we shall present and analysehe anatomical concepts written by Avicenna (Ibn Sina,80—1037 AD) in his famous book the Canon of Medicine andompare them to modern understanding in human anatomy.

rief biography of Avicenna

bu Ali Al-Hossein ibn Adbullah Ibn Sina (known as Avicennan the West) (Fig. 2) was born in a village near Bukhara inugust 980 AD and passed away in Hamadhan in June 1037 AD8—10]. He was the greatest physician in Persia. He alsoerved as philosopher, astronomer, administrator and gov-rnor [11,12]. He composed the Al-Qanun fı al-t.ibb (Theanon of Medicine), which is among the most famous books

n the history of medicine [13,14]. Avicenna’s penchant forategorizing becomes immediately evident in the Canon ofedicine, which is divided into five books [15]. The Canonf Medicine was translated into Latin by Gerard of Cremonan the 12th century [14,16]. The book became the main text-

ook of medicine in the Western and Persian universities10].

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P. Mazengenya, R. Bhikha

natomy and functions of the arteries

eneral description

bn Sina described the distribution arteries throughout theuman body (Fig. 3) and them as vessels originating fromhe top part of the left cavity of the heart, consisting ofwo covering layers (tunics) and capable of pulsation. Heuggested that the inner layer of the arteries was suscepti-le to damage by direct abrasive forces of the flowing bloodnd also by pulsations [17—19]. From the heart two majoressels sprout out of the right and left ventricular infundibu-um leading into the pulmonary artery and aorta respectively20]. Arteries are further classified into large sized elasticrteries, medium sized muscular arteries and small sizedrteries and arterioles [21]. This classification depends onhe closeness to the heart, the pressure of blood carriedy the arteries and the amount of elastic fibres and muscleissue in the walls. Avicenna noticed that the thickness ofhe arteries varies with the demands subjected to a vessel17—19]. He suggested that the aorta was thicker and largerecause it has to deliver blood to large and distant organshile the pulmonary artery (which he named the venousrtery) was thinner because it only served the lungs [17,18].

natomy of the pulmonary artery

onsistent with previous scholars Galen (129—207 AD.) andbu Bakr Mohammed Zakariya Razi, known as Rhazes865—925 AD.), Avicenna erroneously described the pul-onary artery as a thin walled artery consisting of a single

unic and he named it venous artery [1,4]. However, heescribed some aspects of the artery such as its origin fromhe thin walled part (right ventricle) of the heart, presencef the semilunar valve at it origin to prevent backflow oflood and distribution of comparatively low pressure bloodo the lungs [17,20]. In addition he mentioned that the vesselarries nutrient rich blood to the lungs [17,18,22].

natomy of the Aorta

vicenna described the aorta as the largest artery in theody. Its term ‘aorta’ was coined by Aristotle (384—322 BC.)1]. Avicenna mentioned that at the aortic origin the vessels guarded by three valves which prevent back flow dur-ng diastole. He also discussed the functions of the valvesy stating that ‘‘Three membranes and their intermedi-te thickness work best, two membranes would be thickernd four membranes would be thinner’’ [17,22]. He furtherostulated that in order to achieve best functions in anytructure or organ, there is need to balance the qualities ofndividual elements (humours) [17,18,22]. Expounding fromazes’ (865—925 AD.) descriptions, Ibn Sina described coro-ary circulation and the orientation of the coronary vessels.e described the first branches of the aorta and their distri-

ranch of the aorta encircles the heart and also supplies itnd the second branch supplies the muscle on the right side

Vascular anatomy by Ibn Sina 63

Figure 1 Schematic drawings of the circulatory system over time showing Galen, Colombo and Harvey’s descriptions. Colombo’sdescription demonstrates arteriovenous anastomoses in the lung and derives from Ibn Sina’s concepts. Images adopted from Aird[4] and slightly modified.

Figure 2 Portraits of Galen (left), Avicenna (middle) and Hippocrates (right). The image was obtained on internet, open sourcecourtesy of Wellcome library.

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Figure 3 An illustration of the arterial pattern of the humanbody and abdominal viscera by Avicenna in the Canon ofMedicine. Image available on internet, open source courtesyo

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f the heart [17,18,22]. The description is congruent to thenatomical disposition of the right and left coronary arteriesncluding their origin from the ascending aorta.

ranches of the aorta

bn Sina described the branching of the aorta into ascend-ng and descending branches. From his description of theranches of the ascending aorta including its arch, Avicennansufficiently described the brachiocephalic trunk which heescribed as ascending branch towards the manubrium andives off the two carotid arteries to the neck and a thirdranch to supply structures around the sternum, first ribs,pper six cervical vertebrae, clavicle, scapula and struc-ures within the arm [17,22]. These erroneous descriptionselp us to understand the difficulties and limitations ofuman dissection during these times. Resources and tech-ical expertise were not as ubiquitous as they are today andodern readers are urged to avoid drawing biased judge-ents when reading some of the information in Canon ofedicine. The aortic arch gives three branches: the bra-hiocephalic trunk, left common carotid and left subclavianrteries [20].

natomy of carotid arteries

vicenna mentioned that the carotid arteries from each sidef the neck divide at the upper end of the neck into ante-ior and posterior branches [17,18,22]. The anterior branch

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urther divides into a deeper branch which supplies theongue and the deeper muscles of the jaw and a superfi-ial branch which courses superficially in front of the ear toupply through several branches the temporal muscles andcalp [17,18]. He also mentioned the anastomosis betweenranches from opposite side in the scalp. The posteriorranch ascends through the neck and enters the cranial cav-ty through the foramen in the temporal bone. In the cranialavity the posterior branch of the carotid artery forms a net-ork at the base of the brain and end by giving branches to

he brain matter, pia- arachnoid and ventricles of the brain17,22]. Ibn Sina’s description clearly delineates the carotidree in the head and neck region of the human. Accord-ng to Moore, Dalley and Agur [20], the common carotidrtery bifurcates at the level of the upper boarder of thehyroid cartilage in the neck into the external and internalarotid arteries. The external carotid artery lies anterioro the internal carotid and it gives branches which supplyhe neck, upper and lower jaw and tongue musculature. Onhe face the artery continues in front of the ear imbeddedn the substance of the parotid, further divides into maxil-ary artery to the upper jaw and related structures and theuperficial temporal artery which distributes to the tempo-al region and scalp except the forehead region. Contraryo Avicenna’s assertions that the posterior branch of thearotid artery gives a small branch to the joints and mus-les of the neck, the internal carotid artery ascends theeck and enters into the cranial cavity through the carotidanal in the petrous part of the temporal bone without giv-ng a branch in the neck. However, Avicenna described theermination of the internal carotid artery into the arterialircle (circle of Willis) at the base of the brain correctlynd further postulated that the arterial network at thease of the brain facilitates maturation of blood before therain can assimilate it [17,18,23,24]. In line with the the-ry of temperament, blood from heart is hot and the brains of cold temperament so for the blood to be of valueo it, it has to be cooled through a network of vessels athe base of the brain [25]. However in contemporary neu-oanatomy, the circle of Willis, apart from facilitating anfficient source of blood to the brain, also helps to equili-rate pressure between the vertebral and carotid arterialystems [26].

natomy to the descending aorta

onsistent with modern anatomic descriptions, Avicennaentioned that the descending aorta for a greater partescends on the left side of the oesophagus and the ver-ebral column and further distally it shift towards the right17,18,20]. At the level of the 12th thoracic vertebra theescending aorta pierces the diaphragm to enter the abdom-nal cavity. Ibn Sina stated that the aorta on crossing theiaphragm it is fixed by fascia to the thoracic vertebra tovoid constriction from the contractions of the diaphragm17,22]. According to Moore, Dalley and Agur [20], the aortaierces the diaphragm at the aortic hiatus which lies at

he level of the 12 thoracic vertebra; the aorta at thisevel is intimately surrounded by the left and right crura ofhe diaphragm and related fascia. Avicenna described andategorised the branches of descending aorta in the tho-

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racic cavity into four groups which include branches to theeach rib, trachea, lungs and the vertebra [17,18,22]. Thedescending aorta gives rise to branches which are orientatedin three planes (embryonic vascular planes) which includethe anterior unpaired visceral branches to the oesophagus,lateral paired visceral branches to the lungs and postero-lateral paired parietal branches to the intercostal spacesexcept to upper two intercostal spaces [20,27]. Regardingthe arterial branches to the vertebra, Avicenna stated thateach branch passes between the ribs to enter the vertebralcolumn and reach the spinal cord [17,18,22]. The lumbar andsacral segments of the spinal cord receive blood from thedescending aorta through the artery of Adamkiewicz whicharises from the left side of the descending aorta between theT8 and L1 vertebra in approximately 70% of cases [28,29].When this artery is damaged or obstructed, it can result inanterior spinal artery syndrome which is associated with lossof urinary and faecal continence and impaired motor func-tion of the legs; sensory function is often preserved to adegree [30].

At or below the level of the diaphragm, Ibn Sina statedthat the descending aorta gives branches to the stomach,liver and spleen [17,22]. This description is consistent withthe branching pattern of the coeliac trunk at the level ofthe 12th thoracic vertebra and below the diaphragm whereit branches into the left gastric artery, common hepaticartery and the splenic artery to supply the correspond-ing organs [20]. In addition Avicenna mentioned a branchfrom the artery to the liver (hepatic artery) which goes tosupply the gallbladder [17,18], corresponding to the cysticartery a branch of the hepatic artery proper to the gallblad-der. Ibn Sina also described braches to the small intestinesand colon which correspond to the Superior mesentericartery and its branches. The blood supply to the kidneysand associated suprarenal glands was explicitly describedin the Canon of Medicine. Avicenna mentioned two arter-ies from the descending aorta to the kidneys which areinvolved in the absorption of excess water from the bloodand an additional smaller artery which distributes to therenal capsule. The suprarenal glands receive blood fromthree sources which include the inferior phrenic arteries,abdominal aorta and renal arteries [20]. The smaller arteryto the renal capsule alluded to by Ibn Sina correspondsto the middle suprarenal artery. Avicenna described theorigin of the right testicular artery from the descendingaorta and left testicular artery from the left renal arterydemonstrating an anomalous pattern of the gonadal vascul-ature. Gonadal vessels often present with various patterns indifferent populations and numerous patterns pertaining toorigin, course and number have been recorded in literature[31,32]. Towards the terminal bifurcation of the abdom-inal aorta, Avicenna described branches to the rectum.The inferior mesenteric artery stems from the abdominalaorta at the level of L3 vertebra and gives branches to thelarge intestines including the rectum [20]. Ibn Sina men-tioned that the descending aorta terminates by diving into

right and left branches which enter the pelvis and thighs.He described the point of bifurcation as representing theGreek letter lambda. The abdominal aorta terminates intothe common iliac arteries which will subsequently give the

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nternal iliac artery to supply the pelvis and its contents andhe external iliac artery which continues into the lower limb.vicenna described the branches to the pelvic organs suchs the bladder and the uterus and also noted the anasto-oses between arteries from opposite sides [17,18,22]. Toemonstrate his explicitly medical expertise, Ibn Sina stud-ed the anatomy of the gravid uterus and its blood supplynd he mentioned that the uterine arteries become promi-ent during pregnancy adjusting to the increased demandsf blood from the developing foetus and then shrink afterhild birth. In the lower limb region, Ibn Sina describedhe course and distribution of the femoral artery. He men-ioned that the femoral artery gives a muscular branch tohe thigh muscles and the artery continues into the leg andeet towards the big toe. In the thigh the femoral arteryives the profanda femoris artery to supply the thigh mus-ulature and the artery continues into the leg and footegions of the lower limb. Avicenna described the accom-anying veins which are associated with femoral arterylong its course in the lower limb and postulated thatrteries and veins are capable of exchanging the moistureith each other [17,18]. The relationship between arter-

es and accompanying veins has been shown to benefitxchange of heat through counter-current multiplier mech-nism [33] and also to facilitate venous pumping throughhe aid of pulsating arteries [34]. The counter-current mul-iplier system facilitates conservation and exchange of heatetween the warm arterial blood and cold venous bloodrom the extremities. In the testes the relationship betweenhe testicular arteries and the pampiniform venous plexuselps to maintain a temperature below the body tem-erature preparing an environment conducive for spermroduction.

natomy and functions of veins

vicenna distinguished veins and arteries, highlighting onhe different topographic locations and structural differ-nces. For example, he mentioned that veins are foundn both superficial and deep locations, whereas arteriesre always deep; arteries pulsate, veins do not and theovering tunics of arteries are denser than those of veinsecause arteries carry blood with high pressure. In line withrevious scholars such as Aristotle and Rhazes, Avicennaelieved that the blood in the arteries was thinner, warmernd contained breath and or animal spirit [4,17,22]. Gen-rally, Avicenna misconceived the pattern of blood flow inhe veins by stating that all veins originated from the livernd they carry nutrient rich blood to the rest of the body17,22]. It is from this misconception that he describedeins as generally draining blood away from the liver andot towards it and also veins as having branches insteadf tributaries. This idea was also carried over from Galenho described open ended circulation where blood flows

o organs; become consumed and contribute to the for-ation of flesh. However, Avicenna modified Galen’s views

nd hinted on closed circulation by describing arteriovenousnastomoses and artery to artery anastomoses. For clarity in

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his review we ignored the direction of blood flow accordingo Ibn Sina but maintained the pattern and distribution ofhe venous channels and compared them to modern under-tanding.

Ibn Sina described the two major venous systems whichnclude the portal vein:

which drains nutrient rich blood from the intestines andaccessory digestive organs to the concave surface of theliver and the vena cava;

which arises from the convex surface of the liver anddistributes blood to the rest of the body [17,18].

natomy of the vena cava

ccording to Ibn Sina, the vena cava originates from hair-likeeins which anastomose freely with branches of the portalein in the substance of the liver and exit the convex surfacef the liver and divides into ascending and descending veins17,18,22]. The ascending vena cava pierces the diaphragmnd divides into two major branches. One branch enters theight ventricle of the heart and the other branch ascendso supply the head and neck, the upper limbs and inter-ostal spaces [17,18]. Regarding the descending vena cava,e mentioned that the vein supplies structures below theiaphragm. From the above description it can be deducedhat Ibn Sina developed his concept from previous mis-onceptions from earlier scientists/anatomists like Galennd Hippocrates and hence the erroneous interpretationf the venous pattern and direction of blood flow in thisegion. According to Moore, Dalley and Agur [20], the infe-ior vena cava drains blood from the structures below theiaphragm including abdominal contents, pelvis region andower extremities to the right ventricle of the heart whereashe superior vena cava drains receives blood from the upperimbs, head and neck and the thoracic region and drain intohe right ventricle of the heart. Blood from the right ventri-le is then channelled to the lungs through the pulmonaryrtery. However, Avicenna described the venous drainage ofhe face through the external jugular vein and he statedhat the vein receives branches from the face, tongue mus-les, jaws and associated muscles and the region of thear. Ibn Sina also described the internal jugular vein ande traced it back into the confluences of sinus in the occip-tal region. He mentioned that ‘‘The internal jugular veinrains the structures inside the skull and its membranes andt the occipital region blood from various areas of the mem-ranes of the brain meet in a spacious place’’ [17,22]. In thepper limbs, Ibn Sina described the venous patterns of botheep and superficial veins without clear elaboration but heentioned the communication between the basilic vein and

he cephalic vein in the cubital fossa through the medianubital vein. The median cubital vein is widely used forenesection in most clinical procedures in modern clinicalettings.

natomy of the inferior vena cava

s mentioned earlier on, Avicenna misinterpreted the direc-ion of flow of blood in the venous system. For easy of

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P. Mazengenya, R. Bhikha

escription we will follow the inferior vena cava distally asescribed by Avicenna and describe its branches and com-are with modern structural anatomy. Ibn Sina mentionedhat the inferior vena cava gives a larger branch to the leftidney that divides into branches to the renal capsule andubstance of the kidney. Similar to renal arteries the brancho the capsule is a suprarenal vein draining the suprarenalland. The right kidney receives several veins which stemndependently from the inferior vena cava [17,18,22]. Avi-enna described the origin of gonadal veins from the leftenal vein on the left and inferior vena cava on the rightnd also mentioned that sometimes both gonadal veinsrise from the right and left renal veins respectively. Thebove description highlights the anatomical variations of theenal and gonadal vessels often encountered in surgery andutopsy dissection and these variations can be explainedased on the intricate development of gonads, kidneys andheir vasculature [31,32].

Distal to renal veins the inferior vena cava gives offranches to the lumbar vertebra and associated abdominaluscles [17,18]. In accordance with Griessenauer, Raborn,

oreman, Shoja, Loukas and Tubbs [35] Ibn Sina noticed thathe inferior vena cava serves the spinal cord through inter-ertebral veins. He also described the termination of thenferior vena cava at the level of the 5th lumbar vertebranto two common iliac veins. Ibn Sina explicitly describedhe tributaries of the internal iliac vein in both males andemales. He mentioned branches from the uterus, blad-er (fundus and neck), rectum and sacrum, vagina andenis. He further traced the distribution of the externalliac vein into the lower limb and also into the anteriorbdominal wall and the epigastrium. In the epigastrium, Avi-enna described the anastomoses between veins from thehest wall and breast region with those from the exter-al iliac/femoral vein and suggested that the anastomosesight serve as a link between the female breast and the

terus [17,18,22]. In this description it can be construed thatvicenna wanted to establish the bases of erotic stimula-ion; growth of breast during menstrual cycle and pregnancyince the functions of hormones was still obscure. Accordingo Moore, Dalley and Agur [20] the anterolateral abdomi-al wall receives blood from the superior epigastric, inferiorpigastric, superficial and deep circumflex vessels and theseessels anastomose freely in the umbilical and epigastricegions. Lastly, Ibn Sina described the superficial and deepeins of the lower limb and their communication. He alsoescribed the location and distribution of the greater andmall saphenous veins medial and lateral to the leg respec-ively. He stated ‘‘that the medial vein (greater saphenous)uns medially and reaches the dorsum of the foot and theig toe’’ [17,18,22].

onclusion

lthough most of the anatomic descriptions of the vascularystem by Avicenna in the Canon of Medicine draw similari-

ies from his predecessors, he introduced his own findingsspecially the description of closed circulation contraryo Galen’s open circulation. Ibn Sina noted anastomosesetween arteries of different sides on organs such as the

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brain, scalp, uterus and bladder. He also described arteri-ovenous anastomoses on brain, vein to vein anastomoses inthe umbilical and epigastric regions and also between deepand superficial veins in the limbs. Clinically if the communi-cation between superficial veins and deep veins in the limbsis blocked a condition called varicose veins develops andit is often associated venous emboli. Additional significantcontribution was that of the topography of arteries in rela-tion to veins especially where he described the closeness ofarteries and veins in order to exchange and preserve heat inlower limbs.

Disclosure of interest

The authors declare that they have no competing interest.

Author contributions

P.M. and R.B. conceptualised the research topic and carriedout literature search; P.M. wrote the initial manuscript; P.M.and R.B. revised the manuscript and P.M. and R.B. approvedthe final draft of the manuscript.

Acknowledgements

The authors are grateful to the librarians at Ibn Sina instituteof Tibb and Faculty of Health Sciences at the University ofWitwatersrand for the provision of the literature material.We also thank Dr Jean-Leigh Kruger for reviewing and proofediting the manuscript.

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