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Introduction
At birth, the proximal part of the umbilical cord contains various types of thin surface vessels near and outside the umbilicus, in addition to the umbilical arteries and vein. These surface vessels are referred to as “persistent vitelline vessels” [1-3], although there is no evidence that they are connected to the root of the midgut mesentery and thereby form a junction between the vitelline and hepatic portal veins. On the other hand, a vein present in and along the umbilical cord is sometimes termed the “umbilical vein” [4]. However, this name can lead to confusion with the true umbilical vein, which arises from the ductus venosus. Moreover, adults with portal vein hypertension often have additional veins near or along the umbilical vein that are termed “para-umbilical veins”, although this is rare in healthy adults [5, 6]. We are unaware of any study that examined whether the para-umbilical veins run along the true umbilical vein in fetuses or whether they develop after birth in the abdominal wall.
Consequently, the aim of this study was to analyze all types of vessels, other than the true umbilical arteries and vein, at, near, and especially outside the umbilicus of midterm human fetuses. Additional research to be published elsewhere examined the persistent vitelline arteries and veins of midterm fetuses.
Materials and Methods
The study was performed in accordance with the provisions of the 2013 revision of the Declaration of Helsinki. Paraffin-embedded histological sections of the abdomen and pelvis of 25 midterm fetuses (gestational age approximately 10–16 weeks, crown-rump length 52–125 mm) were examined. All sections were part of the large collection at the Department of Anatomy of the Universidad Complutense (Madrid), and the embryos were from miscarriages or ectopic pregnancies at the Department of Obstetrics of the University. No information was available on the genetic background of the embryos or the abortion. The sections were stained with hematoxylin and eosin (H&E), Azan, or Goldner-Masson trichrome. Goldner-Masson trichrome stain [7] shows collagenous fibers in light green, instead of aniline-blue (as in Masson trichome). The sectional planes were horizontal (15 fetuses) or sagittal (10 fetuses) and section thickness ranged from 5 to 10 μm. Each specimen had one umbilical vein and two umbilical arteries, and none had absent or supernumerary vessels. This study was approved by the Ethics Committee of Complutense University (B08/374). All histological photographs were taken using a Nikon Eclipse 80i (Nikon, Tokyo, Japan).
Results
Umbilical branch of the inferior epigastric artery
An arterial branch (the umbilical branch) was consistently present, and it arose from the rectus abdominis. In 5 of 25 fetuses, the arterial branch entered the umbilical cord at 2 to 3 mm from the future umbilicus (Figs. 1A, C, E, 2F, G, 3C). This arterial branch in the cord did not tightly attach to the umbilical artery (Fig. 1F). At the gestational stage of the examined specimens, the superior epigastric artery did not reach the umbilicus because this region was restricted in the superior side of the uppermost tendinous intersection of the rectus abdominis muscle (Fig. 4C, D). Therefore, the umbilical branch originated from the inferior epigastric artery, and the inferior epigastric artery accompanied veins and lymphatic vessels in the rectus abdominis (Fig. 4E). However, the umbilical branch did not accompany veins in the umbilical cord (Fig. 1B, D) nor at the umbilicus (Fig. 2F, G).
Vitelline vein remnants
The vitelline vein remnant in 5 of 25 fetuses originated from the umbilical cord, ran through the peritoneal cavity between the liver and jejunum, and attached to the pancreatic head or duodenum (Figs. 2B, E, 3A–D). In these five specimens, the venous remnant did not take a long course in the cord, and disappeared near the umbilicus. The venous lumen was obliterated to various degrees (Fig. 3G, H), and the venous remnant did not connect to any other vessel such as a para-umbilical vein (see below) and a cutaneous vein.
Thin artery along the umbilical vein
The left hepatic artery always issued one or two thin arteries that ran along the umbilical vein. However, the thin artery reached the umbilicus in only 4 of 25 fetuses (Fig. 5A), but did not enter the umbilical cord and did not communicate with a branch of the inferior epigastric artery.
Venous tributary of pelvic veins along the umbilical artery and/or allantois
The pelvic vein tributaries were well-developed along the proximal part of the umbilical artery (Fig. 1G), but they usually drained the urinary bladder and its continuation, the proximal part of the allantois. The pelvic vein tributary reached a peripheral site at or near the umbilicus in only a few fetuses (Fig. 2D).
Para-umbilical vein running along the umbilical vein
The so-called “para-umbilical vein” ran along the umbilical vein and drained into thin veins at the porta hepatis. This vein was consistently present along the proximal part of the umbilical vein (Fig. 5B, C), but reached the site at or near the umbilicus in only 2 of 25 fetuses (Fig. 5A). Conversely, veins in most sections although they usually appeared as spotty subcutaneous hemorrhages until fixation (Figs. 4D, 5A).
Pelvic lymphatic vessels coming along the umbilical artery
The lymphatic plexus was consistently present along the urinary bladder and allantois, near the umbilicus. Moreover, bilaterally thick lymphatic vessels ran along the lateral or anterior aspect of the umbilical artery in most fetuses (Fig. 5D); they were distinguishable from veins by a cluster of primitive lymphocytes (initial lymph nodes) in the lumen (Fig. 5E, F). Lymphatic vessels along the umbilical artery extended to the umbilicus in most fetuses (Figs. 2A, C, 3D, E, 5A).
Discussion
Our results suggest that various types of thin vessels were present at the fetal umbilicus. The umbilical branch of the inferior epigastric artery was consistently present, and our results may be the first to show that this artery ran into the umbilical cord. In the rectus abdominis, the inferior epigastric artery accompanied the thick vein and lymphatic vessels. However, the arterial branch near the umbilical cord did not accompany veins or lymphatic vessels. We identified the vitelline vein remnant based on its intra-abdominal course. The so-called “para-umbilical vein” rarely reached the umbilicus and made no anastomosis with the pelvic vein tributaries. However, venous drainage of the umbilicus was mostly via the abdominal cutaneous veins. Although the placenta contains no lymphatic tissues [8], it is likely that thick lymphatic vessels along the umbilical artery drained the umbilical cord at and near the umbilicus. These thick lymphatic vessels are presented in classical textbooks of anatomy, as described by Monie [9]. Because of their thickness, even in adults, an internal hernia is likely under the superior vesical artery (a continuation of the umbilical artery) after lymphadenectomy [10].
Clarke [11] and Malas et al. [12] report that the umbilical arteries carried multiple vasa vasorum (7–9 on average) in the arterial wall, and that they maintained the thick wall. However, we found no evidence that the intramural vessel connected to the umbilical branch of the inferior epigastric artery and vein. However, Malas et al. [12] perform a histological examination of the umbilical artery between the umbilicus and superior vesical artery, but we examined sites at and outside of the umbilicus (Figs. 1, 2). Likewise, Clarke [11] performs dye injection into the umbilical artery and demonstrates thin arterial twigs of the thick wall of the “intra-abdominal umbilical artery”. Therefore, the vasa vasorum seemed to be rare in the umbilical cord. Moreover, their descriptions indicated the supplying artery did not originate from the inferior epigastric artery, but instead originated from the umbilical artery itself. The vasa vasorum of the umbilical arteries may be derived to varying degrees from a thin recess of the arterial lumen, due to the specific structure termed the “subendothelial cushion” [9].
Our group previously describes a fibrous umbilical ring in late-term fetuses [13]. However, this fibrous ring or the rim of the fetal umbilicus rarely contained vessels. Instead, the tight fibrous tissue seemed to obliterate the thin vessels that we identified in the mid-term fetuses of the present study. Indeed, for infants and children, recent descriptions of surgical techniques seem to ignore the supernumerary or variant vessels at the umbilicus [14, 15]. Likewise, the so-called “para-umbilical vein” reported in healthy adults [5, 6] might not correspond to the fetal structure, but instead to a secondary vein that develops postnatally in the subperitoneal loose tissue behind the anterior abdominal wall. Moreover, the para-umbilical vein in healthy adults does not always run through the falciform ligament. The para-umbilical collateral vein, which is associated with portal vein hypertension in adults, might develop outside the fibrous umbilical ring.
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