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Table of Contents
ORIGINAL ARTICLE
Year : 2021  |  Volume : 9  |  Issue : 3  |  Page : 108-113

Stereological and histological assessment of the umbilical cord in new-born rat


1 Department of Histology and Embryology, Medicine Faculty, Okan University, Istanbul, Turkey
2 Department of Histology and Embryology, Medicine Faculty, Karabuk University, Karabuk, Turkey

Date of Submission30-Mar-2020
Date of Decision27-Apr-2020
Date of Acceptance19-Jun-2020
Date of Web Publication09-Nov-2020

Correspondence Address:
Ahmad Yahyazadeh
Department of Histology and Embryology, Faculty of Medicine, Karabuk University, Karabu
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/JMAU.JMAU_14_20

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  Abstract 


Background: Umbilical cord plays a crucial role in the continuation of pregnancy by transferring nutrition and oxygen across the placenta to the fetus. We aimed to investigate the morphometrical and histological features of the umbilical cords in new-born rats. Materials and Methods: The adult male and female rats were chosen for matting purpose in the present study. Briefly, ten adult Wistar albino rats (female, n = 5; male, n = 5) were randomly assigned into five groups of two animals (female, n = 1; male, n = 1). Immediately after parturition, two umbilical cords of new-born rats (0-day-old) from each group were randomly selected. Finally, ten umbilical cord samples were examined using the histological and stereological methods in the light and electron microscopes. Results: The total numbers of Hofbauer cells and mesenchymal stromal cells was estimated statistically. We also calculated the mean volume of umbilical cords, arteries and veins, as well as arterial and venous lumens. Our histological findings also exhibited the histological features of Hofbauer cells, mesenchymal stromal cell cells, and blood vessels. Conclusion: Our findings showed more detailed information about umbilical cord tissues and their components, and that may contribute to the diagnose of umbilical cord complications in the developing fetus.

Keywords: Hofbauer cell, mesenchymal stromal cell, new-born rat, stereology, umbilical cord


How to cite this article:
Altunkaynak BZ, Yahyazadeh A. Stereological and histological assessment of the umbilical cord in new-born rat. J Microsc Ultrastruct 2021;9:108-13

How to cite this URL:
Altunkaynak BZ, Yahyazadeh A. Stereological and histological assessment of the umbilical cord in new-born rat. J Microsc Ultrastruct [serial online] 2021 [cited 2021 Nov 28];9:108-13. Available from: https://www.jmau.org/text.asp?2021/9/3/108/300279




  Introduction Top


The umbilical cord, the fetal supply line, is a conduit between the placenta and embryo. This birth cord also contains two prominent arteries and a vein buried into Wharton's jelly (embryonic connective tissue). Wharton's jelly consists of rich collagen-containing ground substance, as well as mesenchymal stromal cell, fibroblast, and macrophage.[1] Furthermore, Wharton's jelly that substitutes for the adventitia of UC vessels can prevent the natal preincidence of mortality through supportive function.[2] In the absence or deficiency of Wharton's jelly, umbilical cord tends to compression, leading to fetal complications.[3],[4],[5],[6] Weissman and Drugan[7] reported that the umbilical cord abnormalities caused the chromosomal aberration. The importance of umbilical cord study may also derived from the presence of potential multipotent stem cells in this vital organ.[8],[9],[10] Mesenchymal stromal cells can be used for therapeutic purposes, which can potentially differentiate into any type of cells.[11],[12] For example, mature types of neurons and glial cells can be differentiated from umbilical cord mesenchymal stromal cell.[13] In the central nervous system, cord blood stem cells can be used in the treatment of the brain injury, stroke, and Cochlear damage.[14],[15],[16] Modified fibroblasts that synthesize collagen fibers contributes to the elasticity of Wharton's jelly, as well as contraction of the vessels.[17] Hence, understanding the architecture features of the umbilical cord helps us to identify its development process and associated abnormalities.

The placenta connects the developing fetus to the uterine wall and provides a natural defense against internal infection through Hofbauer cells. Furthermore, Hofbauer cell, as a placental macrophage, has substantial function in placental pathophysiology.[18]

Despite the importance of the umbilical cord, there are few studies regarding morphometrical assessment of its main structures. We therefore decided to investigate the morphometrical and histological features of the umbilical cords and its main components such as arteries and vein, as well as their lumens. Moreover, fine structures of blood vessels and Hofbauer cells, as well as mesenchymal stromal cells were examined using the electron microscope and light microscope.


  Materials and Methods Top


Experimental procedure and animal care

Ethical approval of the present study was granted by the Experimental Animal Research and Application Centre of Ataturk University, Erzurum, Turkey (No. 1). Ten adult Wistar albino rats (five females and five males), weighing 200–250 g and 12-week-old, were purchased from the Experimental Animal Research and Application Centre of Medicine Faculty of Ataturk University. In each plastic cages, two rats (one female and one male) were housed for 2 days. After the visualization of vaginal plug on the 3rd day, female rats diagnosed as pregnant were removed, then placed individually in 5 cages during the 21-day gestation period. After the delivery, the umbilical cords of two pups from each mother were randomly selected and immediately dissected. Finally, a total of ten umbilical cords were obtained for the stereological and morphometrical analysis. During the experiment period, all rats were maintained under 12:12 h night/day cycle at 50% ± 5% humidity and 22°C ± 2°C. Animals had ad libitum access to food and water.

Histological study

Dissected umbilical cord samples were fixed in 3% glutaraldehyde in a 0.1 M phosphate buffer, followed by the postfixation in 1% osmium tetroxide in 0.1 M phosphate buffer. These samples were dehydrated through graded acetone series, then washed in propylene oxide. Subsequently, samples were embedded in Araldite CY 212.[19],[20] Semi-thin (1 μm thick) and ultra-thin sections (80 nm thick) were cut using a Leica RM2125RT microtome (Gaintenbain Comp., Ankara, Turkey) and ultramicrotome (Nova LKB, Bromma, Sweden), respectively. Semi-thin sections were stained with toluidine blue for the stereological and histological examination in the light microscope.[21],[22] Furthermore, ultra-thin sections were stained with uranyl acetate and lead citrate, then analyzed using a Jeol 100 SX electron microscope (Jeol; Tokyo, Japan).[19]

Stereological study

The point-counting grid and Cavalieri methods were used to estimate the mean volume of the regions of interest [Figure 1]a and [Figure 1]b.[23],[24],[25] For this purpose, a pilot study was designed to survey whether the point density of a grid was valid. The coefficient of variation and coefficient of error were estimated according to the formulas as described by Kurtoglu et al.[26] Briefly, all sections were photographed, then transferred to the private computer. The calibrated grid was randomly superimposed on the photographs, and sum of the points hitting the sections were counted. Finally, the mean volume of the region of interest was calculated as:
Figure 1: Representative micrographs showing application of the Cavalieri principle (a and b) and physical dissector (c and d). (a and b), point-counting grids for applying the Cavalieri principle; (c and d), consecutive pair sections for applying the physical dissector; c, reference section; d, look-up sections; White arrows, countable Hofbauer cell profiles as dissector particle; Black arrow, uncountable profiles according to the rule of unbiased counting frame

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Where, “t” is the total thickness of all sections plus intervals, and “ΣA” is the total area of interest region in all sections.



Where, “a(p)” is the area of point interval, and “ΣP” is the number of points hitting the region of interest.

The total number of Hofbauer and mesenchymal stromal cells was calculated by means of the physical dissector method [Figure 1]c and [Figure 1]d.[25] Consecutive pair sections were chosen using the systematic random sampling technique, which the first section of pair was reference and the other was look up.[27] After photographing the dissector pairs, an unbiased counting frame was placed on micrographs. Then, the profiles of the cells were counted according to the physical disector rules using ImageJ soft program.[23] The numerical density of Hofbauer and ME cells was calculated as:[28]



Where, “ΣQ” is the Hofbauer and ME cell number and “ΣV” is the total volume of the dissector frames in reference sections.

Finally, the total number of Hofbauer and ME cells were calculated using the following formula:



Where, “NV” is numerical density of Hofbauer and ME cells and “VRef” is the mean volume of umbilical cord.

Statistical analysis

Statistical analysis was performed using the IBM version 25.0 SPSS software (SPSS Inc., Chicago, IL, USA). Descriptive statistics were applied for obtaining the mean and standard deviation (SD) values. The results were expressed as mean ± SD.


  Results Top


Stereological results

Our stereological results are given in [Table 1] and [Table 2]. The physical dissector and Cavalieri methods were used for estimating the total number of Hofbauer and mesenchymal stromal cells, as well as the mean volume of umbilical cords.
Table 1: The mean volume of umbilical cords, arteries, and veins as well as arterial and vein lumens

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Table 2: The total number of Hofbauer and mesenchymal stromal cells

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We found that the mean volume of the umbilical cords was 0.58 cm3. Moreover, the mean volumes of arteries and veins were 0.1 cm3 and 0.06 cm3, respectively. Furthermore, the mean lumen volume of arteries and veins was 0.04 cm3 and 0.03 cm3, respectively. We found that the mesenchymal tissue volume was 0.36 cm3 [Table 1].

The total number of Hofbauer and mesenchymal stromal cells were 6327 and 29678, respectively [Table 2].

Histological results

Ultra-structures of blood vessels, Hofbauer, and mesenchymal stromal cells were examined using the electron microscope. We detected the spindle-shaped endothelial cells of blood vessels with prominent ovoid nuclei. The cells observed in tunica media also consisted of a nucleus and distinctive nucleolus, as well as abundant cytoplasm [Figure 2]. Mesenchymal stromal cells (Fibroblast-like cells) of mesenchymal tissue exhibited abundant cytoplasm and euchromatic nucleus [Figure 3]. In Hofbauer cells, the marginalized nucleus and cytoplasmic vacuoles with central location were evident [Figure 4].
Figure 2: Representative micrographs of semi-thin section (a; ×40; bar, 12.5 μm) and ultra-thin sections (b, ×6000; bar, 1 μm) obtained from blood vessel wall of umbilical cord. a, wall of the umbilical artery; b, mesenchymal stromal cells

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Figure 3: Representative micrographs of semi-thin (a, ×40; bar, 12.5 μm) and ultra-thin (b, ×6000; bar, 1 μm) sections obtained from the umbilical cord. Arrow, mesenchymal stromal cells; a and b, mesenchymal stromal cells at the light and electron microscopic levels, respectively

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Figure 4: Representative micrographs of semi-thin (a, ×40; bar, 12.5 μm) and ultra-thin (b, ×6000; bar, 1 μm) sections obtained from the umbilical cord. Arrow, Hofbauer cells; a and b, Hofbauer cells at the light and electron microscopic levels, respectively

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  Discussion Top


Umbilical cord contributes to establish the bidirectional bloodstream between the fetus and mother during pregnancy. Numerous studies have been conducted on the characteristics of the umbilical cord, but comprehensive information regarding the histological structure of umbilical cords and its cells is very limited.[29],[30],[31],[32]

Wharton's jelly that originates from extraembryonic mesoblast is composed of large amounts of extracellular matrix and low number of cells.[1],[33] Stromal cells of Wharton's jelly regulate the umbilical cord blood flow and possess multipotent properties than other stem cells.[34] Lack of Wharton's jelly, which plays a substantial role in fetal growth, can cause fetal death.[13],[35],[36] Hew and Keller[37] suggested that morphological alterations of small laboratory animals occurred faster than human.

Earlier studies that are performed on umbilical cord structures have been based on more clinical approaches such as ultrasonography.[38],[39],[40] Moreover, less quantitative investigations have been carried out on the umbilical cords by means of the unbiased stereological method. Hence, in this study, stereological investigation and histological examination was conducted on the umbilical cord tissues to obtain the novel findings.

To the best of our knowledge, this is the first stereological study that estimates the number of Hofbauer cells and mesenchymal stromal cells, as well as the mean volume of umbilical cords in the rat. Furthermore, there are a few studies concerning histological assessment on the umbilical cord tissues at the electron microscopic and light microscopic level. Our morphometric results provided important information about the volume ratios of all parameters to umbilical cord. This ratio was approximately 62% for mesenchymal tissue, 0.17% arteries, 10% vein, 0.7% arterial lumen and 0.4% vein lumen. We also calculated the ratio of Hofbauer to mesenchymal stromal cells, which was approximately 21%.

Evaluation of the histological architecture of umbilical cord is very important due to the vital role in the fetal development. The previous studies showed that the average diameter and circumference of the umbilical cord after birth were 1.5 cm and 3.6 cm, respectively.[41],[42] It has been reported that there are a relationship between umbilical cord diameter and change in placental features. Proctor et al.[43] reported that thin walled umbilical cord caused some complications such as fetal distress and low placental weight, as well as low infant birth weight. Togni et al.[44] documented that any alteration in the mucous connective tissue of umbilical cord resulted in fetal disorders. Besides, architectural change in the umbilical cord may cause fetal intrauterine growth retardation, leading to undesirable pregnancy outcomes.[45] Accordingly, umbilical cord as a crucial organ acts as a life-saving structure for embryo during pregnancy.

Our histological findings exhibited normal appearance of structures in the umbilical cord tissues. We observed the healthy ultrastructure of blood vessels and mesenchymal stromal cells, as well as Hofbauer cells. The spindle-shaped endothelial cells with ovoid nucleus were detected in blood vessels. The cells in the tunica media possessed the prominent nucleus, nucleolus, and a large amount of cytoplasm. We also found mesenchymal stromal cells (Fibroblast-like cells) with the euchromatic nucleus, a distinct nucleolus and abundant cytoplasm. Ceylan et al.[46] reported the high transcriptional activity of mesenchymal stromal cells due to their spheroid polygonal morphology. These cells exhibited the large number of free ribosome, Golgi complexes, mitochondria, and polestomes. They also detected the enlarged granular endoplasmic reticulum around the nucleus. Qiao et al.[47] documented two different ultrastructural features of mesenchymal stromal cells in human umbilical cords. The one contained a large and oval or round nucleus with one prominent nucleolus, as well as organelle-poor cytoplasm. The other possessed one or two nuclei, organelle-rich cytoplasm, and expansion of mitochondria. Leeson and Leeson[48] investigated the ultrastructure of rat umbilical cords mesenchymal stromal cell at different days gestation. At 17 days gestation, ribosomes attached to well-developed endoplasmic reticulum were observed as polysomal aggregates. At 21 days gestation, they also found less prominent ribosomes than the earlier stage, and these were in the form of certain bundles.

In Hofbauer cells, we found the cytoplasmic vacuoles, as well as marginalized nucleus with central location. The earlier studies have reported important information about the architectural features of Hofbauer cells. These large cells possess both smooth and rough endoplasmic reticulum, ribosomes, numerous rod-shaped mitochondria, and a poorly developed Golgi complexes.[49] Some properties of Hofbauer cells are similar to macrophages in some futures, such as abundant micro- and macro-pinocytotic vesicles, cytoplasmic processes, larger vacuoles (phagosome), and very dense granules.[49],[50] Cytoplasmic granules are thought to be lysosomes due to the activity of phosphatase acid.[51] This system of phagosomes and pinocytotic vesicles plays an important role in pinocytosis and phagocytosis.[49]

We believed that increasing our knowledge of the umbilical cord structures had an important role in the prevention of fetal malformation and abnormality due to histological disorder in the umbilical cord; in this regard, further examinations should therefore be carried out.


  Conclusion Top


The present study showed more detailed information regarding the morphometrical and histological features of umbilical cord than earlier reports. We found the quantitative data about the total number of Hofbauer and mesenchymal stromal cells in the healthy animal group. Moreover, the mean volumes of the umbilical cords, mesenchymal tissue, arteries, and veins were estimated.

Financial support and sponsorship

This article was financially supported by the personal expenses of the authors.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Sobolewski K, Bańkowski E, Chyczewski L, Jaworski S. Collagen and glycosaminoglycans of Wharton's jelly. Biol Neonate 1997;71:11-21.  Back to cited text no. 1
    
2.
Labarrere C, Sebastiani M, Siminovich M, Torassa E, Althabe O. Absence of Wharton's jelly around the umbilical arteries: An unusual cause of perinatal mortality. Placenta 1985;6:555-9.  Back to cited text no. 2
    
3.
Silver RK, Dooley SL, Tamura RK, Depp R. Umbilical cord size and amniotic fluid volume in prolonged pregnancy. Am J Obstet Gynecol 1987;157:716-20.  Back to cited text no. 3
    
4.
Araujo E Jr., Palma-Dias R, Martins WP, Reidy K, da Silva Costa F. Congenital heart disease and adverse perinatal outcome in fetuses with confirmed isolated single functioning umbilical artery. J Obstet Gynaecol 2015;35:85-7.  Back to cited text no. 4
    
5.
Caldas LM, Liao A, Carvalho MH, Francisco RP, Zugaib M. Should fetal growth be a matter of concern in isolated single umbilical artery? Rev Assoc Med Bras (1992) 2014;60:125-30.  Back to cited text no. 5
    
6.
Puvabanditsin S, Garrow E, Bhatt M, Kathiravan S, Gowda S, Wong R, et al. Four-vessel umbilical cord associated with multiple congenital anomalies: A case report and literature review. Fetal Pediatr Pathol 2011;30:98-105.  Back to cited text no. 6
    
7.
Weissman A, Drugan A. Sonographic findings of the umbilical cord: Implications for the risk of fetal chromosomal anomalies. Ultrasound Obstet Gynecol 2001;17:536-41.  Back to cited text no. 7
    
8.
Li WW, Wei YH, Li H, Lai DM, Lin TN. Isolation and characterization of a novel strain of mesenchymal stem cells from mouse umbilical cord: Potential application in cell-based therapy. PLoS One 2013;8:e74478.  Back to cited text no. 8
    
9.
Jomura S, Uy M, Mitchell K, Dallasen R, Bode CJ, Xu Y. Potential treatment of cerebral global ischemia with Oct-4+umbilical cord matrix cells. Stem Cells 2007;25:98-106.  Back to cited text no. 9
    
10.
Wang HS, Hung SC, Peng ST, Huang CC, Wei HM, Guo J, et al. Mesenchymal stem cells in the Wharton's jelly of the human umbilical cord. Stem Cells 2004;22:1330-7.  Back to cited text no. 10
    
11.
Wu YM, Cao YB, Li XH, Xu LX, Liu ZY, Liu B, et al. Transplantation of umbilical cord mesenchymal stem cells combined with haploidentical hematopoietic stem cells for 36 patients with refractory/relapsed myeloid leukemia. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2014;22:1053-7.  Back to cited text no. 11
    
12.
Chao KC, Chao KF, Fu YS, Liu SH. Islet-like clusters derived from mesenchymal stem cells in Wharton's Jelly of the human umbilical cord for transplantation to control type 1 diabetes. PLoS One 2008;3:e1451.  Back to cited text no. 12
    
13.
Mitchell KE, Weiss ML, Mitchell BM, Martin P, Davis D, Morales L, et al. Matrix cells from Wharton's jelly form neurons and glia. Stem Cells 2003;21:50-60.  Back to cited text no. 13
    
14.
Cotten CM, Murtha AP, Goldberg RN, Grotegut CA, Smith PB, Goldstein RF, et al. Feasibility of autologous cord blood cells for infants with hypoxic-ischemic encephalopathy. J Pediatr 2014;164:973-90.  Back to cited text no. 14
    
15.
Revoltella RP, Papini S, Rosellini A, Michelini M, Franceschini V, Ciorba A, et al. Cochlear repair by transplantation of human cord blood CD133+cells to nod-scid mice made deaf with kanamycin and noise. Cell Transplant 2008;17:665-78.  Back to cited text no. 15
    
16.
Vendrame M, Gemma C, Pennypacker KR, Bickford PC, Davis Sanberg C, Sanberg PR, et al. Cord blood rescues stroke-induced changes in splenocyte phenotype and function. Exp Neurol 2006;199:191-200.  Back to cited text no. 16
    
17.
Takechi K, Kuwabara Y, Mizuno M. Ultrastructural and immunohistochemical studies of Wharton's jelly umbilical cord cells. Placenta 1993;14:235-45.  Back to cited text no. 17
    
18.
Tang Z, Abrahams VM, Mor G, Guller S. Placental Hofbauer cells and complications of pregnancy. Ann N Y Acad Sci 2011;1221:103-8.  Back to cited text no. 18
    
19.
Yahyazedeh A, Altunkaynak BZ, Akgül N, Akgül HM. A histopathological and stereological study of liver damage in female rats caused by mercury vapor. Biotech Histochem 2017;92:338-46.  Back to cited text no. 19
    
20.
Bekar E, Altunkaynak BZ, Balcı K, Aslan G, Ayyıldız M, Kaplan S. Effects of high fat diet induced obesity on peripheral nerve regeneration and levels of GAP 43 and TGF-β in rats. Biotech Histochem 2014;89:446-56.  Back to cited text no. 20
    
21.
Bancroft JD, Cook HC, Stirling RW. Manual of Histological Techniques and their Diagnostic Applications. London: Churchill Livingstone; 1994. p. 457-8.  Back to cited text no. 21
    
22.
Harorli OT, Bayindir YZ, Altunkaynak Z, Tatar A. Cytotoxic effects of TEGDMA on THP-1 cells in vitro. Med Oral Patol Oral Cir Bucal 2009;14:e489-93.  Back to cited text no. 22
    
23.
Altunkaynak BZ, Akgül N, Yahyazedeh A, Makaracı E, Akgül HM. A stereological study of the effects of mercury inhalation on the cerebellum. Biotech Histochem 2019;94:42-7.  Back to cited text no. 23
    
24.
Yahyazadeh A, Altunkaynak BZ. Protective effects of luteolin on rat testis following exposure to 900 MHz electromagnetic field. Biotech Histochem 2019;94:298-307.  Back to cited text no. 24
    
25.
Yahyazadeh A, Altunkaynak BZ. Investigation of the neuroprotective effects of thymoquinone on rat spinal cord exposed to 900 MHz electromagnetic field. J Chem Neuroanat 2019;100:101657.  Back to cited text no. 25
    
26.
Kurtoglu E, Altunkaynak BZ, Aydin I, Ozdemir AZ, Altun G, Kokcu A, et al. Role of vascular endothelial growth factor and placental growth factor expression on placenta structure in pre-eclamptic pregnancy. J Obstet Gynaecol Res 2015;41:1533-40.  Back to cited text no. 26
    
27.
Ulubay M, Yahyazadeh A, Deniz ÖG, Kıvrak EG, Altunkaynak BZ, Erdem G, et al. Effects of prenatal 900 MHz electromagnetic field exposures on the histology of rat kidney. Int J Radiat Biol 2015;91:35-41.  Back to cited text no. 27
    
28.
Altunkaynak BZ, Akgül N, Yahyazadeh A, Altunkaynak ME, Turkmen AP, Akgül HM, et al. Effect of mercury vapor inhalation on rat ovary: Stereology and histopathology. J Obstet Gynaecol Res 2016;42:410-6.  Back to cited text no. 28
    
29.
Romanowicz L, Bańkowski E. Altered sphingolipid composition in Wharton's jelly of pre-eclamptic newborns. Pathobiology 2010;77:78-87.  Back to cited text no. 29
    
30.
Stehbens WE, Wakefield JS, Gilbert-Barness E, Zuccollo JM. Histopathology and ultrastructure of human umbilical blood vessels. Fetal Pediatr Pathol 2005;24:297-315.  Back to cited text no. 30
    
31.
Raio L, Ghezzi F, Di Naro E, Duwe DG, Cromi A, Schneider H. Umbilical cord morphologic characteristics and umbilical artery Doppler parameters in intrauterine growth-restricted fetuses. J Ultrasound Med 2003;22:1341-7.  Back to cited text no. 31
    
32.
Di Naro E, Ghezzi F, Raio L, Franchi M, D'Addario V. Umbilical cord morphology and pregnancy outcome. Eur J Obstet Gynecol Reprod Biol 2001;96:150-7.  Back to cited text no. 32
    
33.
Schke KB, Famann PK. Anatomy and pathology of umbilical cord and major fetal vessels. In: Benirschke K, Kaufmann P, editors. Pathol of Human Placenta. 4th ed.. New York: Springer; 2000. p. 337-8, 362-4.  Back to cited text no. 33
    
34.
Can A, Karahuseyinoglu S. Concise review: Human umbilical cord stroma with regard to the source of fetus-derived stem cells. Stem Cells 2007;25:2886-95.  Back to cited text no. 34
    
35.
Blanco MV, Vega HR, Giuliano R, Grana DR, Azzato F, Lerman J, et al. Histomorphometry of umbilical cord blood vessels in preeclampsia. J Clin Hypertens (Greenwich) 2011;13:30-4.  Back to cited text no. 35
    
36.
Schwarz W. A study on the structure, function and the behaviour of the umbilical cord, particularly of the Wharton's jelly; experimental research. I. Z Geburtshilfe Gynakol 1955;144:1-33.  Back to cited text no. 36
    
37.
Hew KW, Keller KA. Postnatal anatomical and functional development of the heart: A species comparison. Birth Defects Res B Dev Reprod Toxicol 2003;68:309-20.  Back to cited text no. 37
    
38.
Ghezzi F, Raio L, Günter Duwe D, Cromi A, Karousou E, Dürig P. Sonographic umbilical vessel morphometry and perinatal outcome of fetuses with a lean umbilical cord. J Clin Ultrasound 2005;33:18-23.  Back to cited text no. 38
    
39.
Meyer WW, Rumpelt HJ, Yao AC, Lind J. Structure and closure mechanism of the human umbilical artery. Eur J Pediatr 1978;128:247-59.  Back to cited text no. 39
    
40.
Raio L, Ghezzi F, Di Naro E, Franchi M, Maymon E, Mueller MD, et al. Prenatal diagnosis of a lean umbilical cord: A simple marker for the fetus at risk of being small for gestational age at birth. Ultrasound Obstet Gynecol 1999;13:176-80.  Back to cited text no. 40
    
41.
Patel D, Dawson M, Kalyanam P, Lungus E, Weiss H, Flaherty E, et al. Umbilical cord circumference at birth. Am J Dis Child 1989;143:638-9.  Back to cited text no. 41
    
42.
Moinian M, Meyer WW, Lind J. Diameters of umbilical cord vessels and the weight of the cord in relation to clamping time. Am J Obstet Gynecol 1969;105:604-11.  Back to cited text no. 42
    
43.
Proctor LK, Fitzgerald B, Whittle WL, Mokhtari N, Lee E, Machin G, et al. Umbilical cord diameter percentile curves and their correlation to birth weight and placental pathology. Placenta 2013;34:62-6.  Back to cited text no. 43
    
44.
Togni FA, Araujo Júnior E, Vasques FA, Moron AF, Torloni MR, Nardozza LM. The cross-sectional area of umbilical cord components in normal pregnancy. Int J Gynaecol Obstet 2007;96:156-61.  Back to cited text no. 44
    
45.
Inan S, Sanci M, Can D, Vatansever S, Oztekin O, Tinar S. Comparative morphological differences between umbilical cords from chronic hypertensive and preeclamptic pregnancies. Acta Med Okayama 2002;56:177-86.  Back to cited text no. 45
    
46.
Ceylan A, Özgenç Ö, Korhan A, Korkusuz P, Özen A. Ultrastructure of rat umbilical cord stroma-derived mesenchymal stem cells. Turk J Vet Anim Sci 2017;41:464-70.  Back to cited text no. 46
    
47.
Qiao SM, Chen GH, Wang Y, Wu DP. Ultrastructure of human umbilical cord mesenchymal stem cells. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2012;20:443-7.  Back to cited text no. 47
    
48.
Leeson CR, Leeson TS. The fine structure of the rat umbilical cord at various times of gestation. Anat Rec 1965;151:183-97.  Back to cited text no. 48
    
49.
Demir R, Erbengi T. Some new findings about Hofbauer cells in the chorionic villi of the human placenta. Acta Anat (Basel) 1984;119:18-26.  Back to cited text no. 49
    
50.
Georgiades P, Ferguson-Smith AC, Burton GJ. Comparative developmental anatomy of the murine and human definitive placentae. Placenta 2002;23:3-19.  Back to cited text no. 50
    
51.
Matsubara S, Minakami H, Yamada T, KoikeT, Izumi A, Takizawa T, et al. Stimulated Hofbauer cells in the placental villi from patients with second trimester abortions. Acta Histochem Cytochem 1998;31:447-52.  Back to cited text no. 51
    


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