Tributaries of the hepatic vein in the ostrich ( Struthio camelus )

The ostrich ( Struthio camelus , Linnaeus 1758) is the largest bird in the world. It is of great economic importance in Africa and is found across several countries. With developments in breeding systems, morphological studies that facilitate the application of the knowledge are necessary, considering the species has unique anatomical features. The objective of the present study was to describe the major tributaries of the hepatic vein in the species. Ten viscera of adult individuals of both sexes, which were injected with Neoprene latex through the hepatic vein, were used to visualize their tributaries. After the vascular repletion, the tissues were fixed and conserved in 10% formaldehyde aqueous solution. The hepatic carrier system was dissected and photo-documented. The left hepatic vein receives blood from the proventricle and gastric ventricle, while the right hepatic vein is responsible for the drainage of blood into the following organs: spleen, through the proventriculosplenic vein; pancreas, through the pancreaticoduodenal vein; jejunum, through the jejunum trunk; and the colon, which forms the cranial mesenteric vein.


Introduction
The ostrich (Struthio camelus, L. 1758) is considered an herbivore (1,2,3) with a gastrointestinal tract that is different from those of domestic birds (1) .In addition, the absence of flight in ratites such as ostriches could have led to a distinction in their digestive tracts (4) .Ostrich, rhea (Rhea americana) and emu (Dromaius novaehollandiae) have different gastrointestinal system anatomies.The ostrich has a well-developed, large, saccular caecum, and a long, partially sacular colon (5,6) .The emu has a small colon, while in the emu, the caecum and colon are small (4,7,8) .
The ostrich diet consists of a variety of succulent plants, grasses, and bushes (1,9) , which allows a morphophysiological adaptation common in herbivorous and granivorous birds; a muscular gizzard full of sand to facilitate the reduction of the sizes of ingested particles (4,10,11) .
Liver blood drainage has implications in various fields of study and has been investigated extensively.In birds, the blood liver drainage systems has been described in ducks (Cairina moschata) (13) , geese (Anser domestica) (14) , domestic pigeons (Columba livia domestica) (15) , egrets (Bubulcus ibis) (16) and Gallus gallus (17,18,19,26) , considering the hepatic system in birds differs from that in mammals.In addition, in birds, the system is anastomous to the renal system (12).The renal portal system has already been described in ostriches.However, to date, this is the first study on the tributaries of the hepatic portal system in the species.

Material and Methods
Ten (10) viscera of adult ostriches, five males and five females, collected at Frigorífico Aravestruz, in the municipality of Araçatuba -SP, were used.After the collection, the viscera were sent to the Animal Morphology Laboratory at the Faculdade de Medicina Veterinária de Araçatuba, UNESP (Faculty of Veterinary Medicine, Araçatuba, Sao Paulo State University).This study was approved by the Ethics Committee on the Use of Animals of the School of Dentistry of Araçatuba/UNESP under the FOA protocol: 00602-2017.In the laboratory, the viscera were washed in running water to remove blood from the veins.Subsequently, the hepatic vein was identified for the injection of Neoprene latex, which has a blue pigment, to fill its tributaries.After the injection, the viscera were submerged in an aqueous solution of 10% formaldehyde for a 48 hours to fix the tissues and solidify the Neoprene latex (20) .After fixation, the visceral block was washed in running water for 24 hours to remove the fixator, and then dissected and photo documented.
The anatomical terms are in accordance with the Anatomical Nomenclature of Birds, Nomina Anatomica Avium (21) .

Hepatic vein
A common hepatic vein, located on the visceral face of liver between the right and left lobes, originated from the union of the right and left hepatic veins.

Left hepatic vein
Two vessels, the ventral proventricular vein and the left proventricular vein, join to form the hepatic vein.Both vessels continue cranioventrally to join the gastric veins.

Right hepatic vein
Much more vessels contributed to the formation of the right hepatic vein than the left hepatic vein.The right hepatic vein was formed by the confluence of the following veins: proventriculosplenic, gastro pancreaticoduodenal, and cranial mesenteric vein.(Figures 1A-B).
The proventriculosplenic vein arises from the confluence of two important veins, the right proventricular vein and the splenic vein, with the latter originating from the ventromedial surface of the spleen (Figures 1B-C).
The gastro pancreaticoduodenal vein is the union of the right and left gastric veins with the pancreaticoduodenal vein.The right gastric vein received branches of the right dorsal and ventral gastric veins at its origin on the right side of the gastric ventricle (Figures 1A-E).
The cranial mesenteric vein was formed by two distinct trunks: the colic trunk and the jejunal trunk, formed by veins that flow from the duodenal, iliac, cecal, and colic regions (Figures 1A).
The jejunal trunk was derived from the duodenal veins, originating from the descending and ascending duodenum; from the ileocecal veins responsible for the drainage of the caecum and ileum (Figures 1A and 1E).
The colic trunk originated from the colic veins, coccigeomesenteric veins, and rectal vein; all originating from the colon and cloaca (Figures 1A and 1D).It is discernible that the configuration of the veins in S. camelus differs from other species, particularly in the colic trunk.
In the ostrich, the left hepatic vein drains the proventricle through the ventral and left proventriculosplenic veins and part of the gastric ventricle through the gastric veins as in G. gallus (17,18,19) , in the egret (B.ibis) (16) and in domestic pigeons (C.livia domestica) (13,15) .In G. gallus (17,18,19,26) , the left hepatic vein is formed by the ventral and left gastric veins and by the proventricular veins (13) .Conversely, in ducks, the left hepatic vein is formed by one or two left gastric veins that drain blood from the ventral margin of the gastric ventricle, in addition to the pyloric and caudal proventricular veins (19) .
The right hepatic vein in ostrich is formed by the confluence of proventriculosplenic, gastro pancreaticoduodenal and cranial mesenteric veins, similar to the descriptions in the chicken (G.gallus domesticus) (24,26) and in heron B. ibis (15) .However, in the domestic duck (C.moschata) (13) , in domestic birds (G.gallus) ( 17,18,19) and in the chicken (G.gallus domesticus) (24,26), the right hepatic vein is formed by the cranial gastro pancreaticoduodenal and mesenteric veins.
The proventriculosplenic vein was formed by the confluence of two important veins: the right proventricular vein and the splenic vein, both merging into the right hepatic vein, which are consistent with the patterns observed in heron (B.ibis) (16) .In the present study, the right proventricular vein received the confluence of the cranial and medial branches draining the cranial and medial third of the proventriculus.
In the ostrich, the spleen is drained by the splenic vein and the proventriculoesplenic vein joining the hepatic vein.In the domestic duck (C.moschata) (13) , the spleen is drained by the splenic vein and the protrichulosplenic vein, which is formed by the union of the splenic and dorsal protrichular veins (17) .In the chicken (G.gallus domesticus) (24) , the right and protriculoesplenic veins join the right hepatic vein via a common trunk, called the protriculusplenic vein, while in the duck (A.anas domesticus) and goose (A.anser domesticus) (22) have been described as two splenic protriculoresplenic veins and one right protriculus vein, which join the right hepatic vein separately.
The gastro pancreaticoduodenal vein was formed by the confluence of right and pancreaticoduodenal gastric veins, which joined ventrally to the right hepatic vein, as reported in G. gallus (17) and the heron (B.ibis) (16) .In the ostrich, a trend similar to that in the domestic duck (C.moschata) was observed (13) , in which the corresponding gastro pancreaticoduodenal vein is formed by the pancreaticoduodenal vein and the two gastric veins and their tributaries (17,19) .
The duodenal veins drained the fasting veins in the fasting trunk and the ileocecal veins, responsible for the regions of the two caeca and the ileum, also flowed into the fasting veins in the ostrich.The cecal vein is formed by the union of branches from the pancreaticoduodenal vein and the pancreatic vein, which differs from the one observed in the egret (B.ibis) (16) , in which the ileal veins converge on the ileocecal vein and end at the caudal mesenteric vein (15) .Another difference observed in relation to the anatomical pattern of the egret (B.ibis) (16) and domestic pigeons (C.livia domestica) (13,15) is that instead of the ostrich's fasting veins draining into the cranial mesenteric vein, they converge into the fasting trunk.In ostriches and other species, the presence of duodenojejunal veins such as those found in ducks (A.anas domesticus) and geese (A.anser domesticus) is not observed (22) .
According to Bezuidenhout (25) , the average total length of the intestine in an adult ostrich is 2390 cm, while that of the colon is 1640 cm, which are very long when compared to the lengths in other ratites such as the rhea and emu.Because the ostrich colon is so extensive, the cranial mesenteric vein is formed from two distinct veins: the jejunal trunk and the colonic trunk.Such confluence of the cranial mesenteric vein differs from that observed in poultry (G.gallus) (17,18,19,26) , duck (C.moschata) (13,14,22) , goose (A.domestica) (13) , domestic pigeon (C.livia domestica) (13,15) , egret (B.ibis) (16) , and domestic goose (A.anser domesticus) (22,23)   .According to the results of the present study, the tributaries of the hepatic vein in ostriches reveal an extension of the jejunum and caecum intestinal structures, revealing unique venous vessels that suggest species-specific angioarchitecture.