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Abstract

Umbilical cord hemangiomas are rare lesions, for which data on pregnancy outcome is lacking. This study combines a multi-institution 4-case series with a systematic literature search (n = 52) to determine possible pathologic lesion parameters which may have an effect on pregnancy outcome. Of all 56 pregnancies, lesion size ranged from 0.2 to 23.0 cm with pregnancy outcomes ranging from healthy liveborns (58.9%), liveborns with severe complications largely due to prematurity and/or fluid overload (12.5%), intrauterine/neonatal demise (25.0%), and pregnancy termination (3.6%). Of the 52 cases included for statistical analysis, there was no significant association between fetal outcome and vascular lesion location (P = .12) or fetal outcome and single umbilical artery involvement versus involvement of other vasculature (P = .29). The mean length of vascular lesions that resulted in healthy liveborns did not significantly differ from those resulting in severe fetal complications and/or demise (P = .72). Cases resulting in severe complications and/or demise were significantly earlier at delivery than those resulting in healthy liveborns (P < .001). Combined findings suggest that functional lesion characteristics, such as the degree of turbulent flow generated, have more significance than size, especially in early gestation losses. Moving forward, standardized reporting of pathologic lesion characteristics is paramount to better predict pregnancy prognosis.

Keywords

umbilical cord hemangioma umbilical cord angiomyxoma placental pathology umbilical cord tumors

Introduction

Umbilical cord hemangiomas are rare lesions that present incidentally on ultrasound or with findings ranging from increased maternal serum alpha-fetoprotein to polyhydramnios, respiratory distress and/or intrauterine fetal demise secondary to hydrops, cord rupture, or cord stenosis. These lesions often manifest varying amounts of extravasated fluid and/or cystic Wharton jelly change due to their resultant turbulent flow, and hence have been occasionally referred to as “angiomyxomas.”

As in any other body site, pathologic diagnosis of a cord hemangioma consists of microscopic visualization of vascular channels lined by simple, cytologically bland endothelial cells that exhibit immunoreactivity for vascular markers such as CD31 and VWF. Use of Glut-1 immunostaining has been suggested to differentiate between hemangiomas of infantile origin and chorangiomas with cord involvement or a true umbilical cord hemangioma arising from remnant vitelline vessels.^1-3

The literature of umbilical cord hemangiomas is limited to single reports over the past 70 years including a historical 4-case series.⁴ Typically, lesion parameters reported included size, degree of cystic change, and involved umbilical vasculature; however, reporting consistency has been spotty. As a result, little is known about their prognosis or any pathologic characteristics that may help predict pregnancy outcome. This multi-institution case series combines 4 new cases with those from the literature to determine the utility of various pathologic lesion parameters toward informing pregnancy prognosis.

Case Series

Following institution ethics approval, we conducted a retrospective search of our electronic pathology databases for relevant cases accessioned 01/01/2010 to 01/01/2022 using the search terms “vascular anomaly of umbilical cord,” “arterial anomaly of umbilical cord,” “venous anomaly of umbilical cord,” “umbilical cord hemangioma,” and “umbilical cord angiomyxoma.” The search yielded 2 cases from Health Science Centre, Winnipeg, Canada, 1 case from Seattle Children’s Hospital, Seattle, USA, and 1 case from the University of Alabama Hospital, Birmingham, USA. Salient clinical and pathologic findings are summarized in Table 1.

Table 1.

Clinical and pathologic characteristics of umbilical cord hemangioma cases by systematic literature search.

Case	Author	Size (cm)	Site	GA (wk)	Vessel(s) involved	Fetal outcome, salient comorbidities
1	This study	11.5	F	37	SUA	Healthy
2	This study	4.3	P	37	SUA	Healthy
3	This study	6.0	P	34	SUA	Healthy
4	This study	23.0	P	37	BUA	Healthy
5	Heifetz and Rueda-Pedraza⁴	NS	NS	40	NS	Healthy
6	Heifetz and Rueda-Pedraza⁴	0.2	NS	39	NS	IUFD, abruption, short cord (40 cm)
7	Seifer et al⁵	NS	F	31	BUA	Compl’s: RDS, twins, hydrops, skin lesions
8	Dombrowski et al⁶	NS	P	NS	VC	IUFD, cord rupture, ileal atresia, patent vitelline duct
9	Heifetz and Rueda-Pedraza⁴	0.5	NS	43	SUA	IUFD, postmaturity
10	Barson et al⁷	1.5	P	20	NS	TOP for raised AFP secondary to hemangioma
11	Armes and Billson⁸	1.5	P	32	BUA	IUFD, twins, limb deformities
12	Sahinoglu et al⁹	1.8	NS	24	NS	IUFD, KTS
13	Miller and Gauderer¹⁰	2.0	F	38	UV	Healthy
14	Malliah et al¹¹	2.0	P	37	NS	Healthy, port wine skin lesions
15	Sathiyasathan et al¹²	2.2	P	26	NS	IUFD
16	Kamitomo et al¹³	2.5	P	17	SUA, UV	IUFD
17	Daniel-Spiegel et al¹⁴	2.5	P	38	WJC	Healthy, port wine skin lesions
18	Matsuda et al¹⁵	2.5	F	39	SUA, UV	Healthy, maternal gestational diabetes
19	Lok et al¹⁶	2.5	F	23	SUA, UV	IUFD, fetal anemia
20	Yu et al¹⁷	2.6	NS	26	SUA	TOP, KTS
21	Iglesias-Deus et al²	3.0	F	40	SUA	Healthy, large SMA hemangioma
22	Resta et al¹⁸	3.2	P	17	BUA	IUFD, cord stenosis
23	Cheng et al¹⁹	3.2	P	38	NS	Healthy
24	Akiba et al²⁰	3.2	F	38	SUA	Healthy
25	Gӧksever et al²¹	3.5	F	38	SUA	Healthy, maternal epilepsy
26	Schwikert et al²²	3.5	P	40	SUA	Compl’s: diffuse neonatal hemangiomatosis
27	Ghidini et al²³	3.7	F	37	NS	Healthy, hypospadias
28	Søndergard²⁴	4.0	P	28	NS	IUFD
29	Vougiouklakis et al²⁵	4.0	F	38	BUA, UV	IUFD, cord rupture
30	Natalucci et al²⁶	4.0	F	38	UV	Healthy
31	Papadopoulos et al²⁷	4.1	M	37	SUA	Healthy
32	Smulian et al²⁸	4.2	F	36	SUA	Compl’s: RDS, pleural & pericardial effusions, positional tachycardia
33	Pollack and Bound²⁹	4.5	P	38	NS	Healthy
34	Jacques and Qureshi³⁰	4.5	P	26	BUA	IUFD, amniotic epithelial inclusion cyst associated with hemangioma
35	Kaur et al³	4.5	F	33	NS	Healthy, following surgical excision and umbilicoplasty
36	Weyerts et al³¹	4.8	F	37	NS	Healthy, anterior wall hemangioma
37	Yavner and Redline³²	5.0	F	38	SUA, UV	Healthy
38	Wilson et al³³	5.0	F	36	NS	Healthy
39	Rocha et al³⁴	5.0	NS	39	NS	Healthy
40	Jakobovits and Herezeg³⁵	5.9	P	32	SUA, UV	Healthy
41	Carvounis et al³⁶	6.0	P	40	SUA	Healthy, hypoplastic umbilical artery
42	Angelico et al³⁷	6.0	M	36	SUA	Healthy
43	Benirschke and Dodds³⁸	7.0	P	39	NS	Healthy, hypoplastic umbilical artery
44	Tekant et al³⁹	7.0	F	38	NS	Healthy, following surgical excision (inserted into umbilicus)
45	Tennstedt et al⁴⁰	8.0	F	36	SUA, UV	Healthy
46	Jauniaux et al⁴¹	8.0	P	37	BUA, UV	Healthy, port wine skin lesions
47	Iyoob et al⁴²	8.0	P	31	NS	Healthy, SUA, maternal preeclampsia
48	Gramellini et al⁴³	9.5	P	40	NS	Healthy
49	Heifetz and Rueda-Pedraza⁴	9.5	P	40	SUA	Healthy
50	Fortune and Ostor⁴⁴	10.0	P	30	NS	IUFD
51	Zhang et al⁴⁵	10.2	P	34	SUA	IUFD, hydrops, polyhydramnios
52	Barry et al⁴⁶	12.0	P	NS	NS	Compl’s: RDS, congenital heart disease, liver angioma
53	Gouin et al⁴⁷	12.0	P	38	NS	Healthy, bilateral choroid plexus cysts
54	Mishriki et al⁴⁸	13.0	P	30	NS	Compl’s: NND, RDS, NEC, hydrocephalus
55	Calderella et al⁴⁹	13.0	P	32	NS	Compl’s: RDS, hydrops, cardiomegaly
56	Hara et al⁵⁰	17.0	P	29	VC	Compl’s: RDS, prematurity, heart failure

Abbreviations: AFP, alpha fetoprotein; BUA, both umbilical arteries; Compl’s, liveborn with complications; F, fetal; GA, gestational age; IUFD, intrauterine fetal demise; KTS, Klippel Trenaunay syndrome; M, midpoint; NEC, necrotizing enterocolitis.; NND, neonatal demise; NS, not specified; P, placental; RDS, respiratory distress syndrome; SMA, superior mesenteric artery; SUA, single umbilical artery; TOP, termination of pregnancy; UV, umbilical vein; VC, vitelline capillaries; WJC, Wharton jelly capillaries.

Case 1

A 36-year-old G1P0 mother was diagnosed on prenatal ultrasound with a 12 cm vascular UC mass. She was closely followed and delivered a healthy infant by Cesarian section at 37 weeks following spontaneous membrane rupture (APGAR score 9 at both 1 and 5 minutes). On gross placental examination, the UC was massively distended by a 11.5 cm tumor located 49 cm from disc insertion (Figure 1(a)). Sectioning revealed associated marked edema and cystic-type change of the Wharton jelly proximal to the lesion. Histologic examination confirmed a cytologically bland endothelial proliferation originating from an umbilical artery (Figure 2(a) and (b)). The endothelial cells were CD34-immunoreactive while negative for Glut-1 (Figure 2(d)) and D2 to 40.

Figure 1.

Placental gross examination in cases of umbilical cord hemangiomas (Case 1: A, Case 3: B) demonstrated massive, well demarcated, fusiform Wharton jelly edema involving a portion of the umbilical cord. Cut section of the lesion in Case 3 revealed nodules arising from an umbilical artery (C).

Figure 2.

Microscopic examination in Cases 1 (H&E A: 20×, B: 400×) and 3 (H&E C: 100×) revealed cytologically bland, GLUT-1 negative (Case 1: D, 400×; Case 3: E, 200×), endothelial cell proliferations in keeping with diagnoses of umbilical cord hemangiomas.

Case 2

A 34-year-old G4P3 mother delivered a healthy infant by Cesarian section at 34 weeks following spontaneous preterm premature membrane rupture and footling breech presentation (APGAR score 9 at both 1 and 5 minutes). Maternal serum screen at 15 weeks had identified increased alpha fetoprotein (92.9 μg/L) and nuchal translucency (1.4 mm); however, prenatal ultrasounds at 12, 16, 21, and 29 weeks were normal. On gross placental examination, there was a 4.3 cm tumor located immediately adjacent to the disc insertion. Histologic examination confirmed a benign endothelial proliferation arising from an umbilical artery.

Case 3

Ultrasonography in a 31-year-old mother at 20 weeks of gestational age demonstrated a large umbilical cord mass with Doppler flow. The mother was closely followed, and labor was induced at 34 weeks. She delivered a healthy liveborn infant. Gross examination revealed a firm, pale pink mass measuring 6 cm in length × 3.5 cm in maximal diameter within the proximal umbilical cord (Figure 1(b) and (c)). Cut surface showed a tumor composed of multiple interconnected nodules within increased Wharton’s jelly, intimately surrounding the umbilical vessels. The mass approached to within 3 mm of the chorionic plate surface, but appeared distinct from it. A separate region of the distal cord, 4 cm from the proximal mass, also displayed massive dilation up to 6 cm for a length of 17 cm, with cystic dilation on cut surface, but was not directly involved by the vascular mass. Dye injection demonstrated perfusion of the mass by 1 umbilical artery, but no connection to the umbilical vein. The other umbilical artery contained thrombi that prevented perfusion. Histologically, the mass displayed a multilobulated vascular proliferation. The majority of the tumor appeared composed of arborizing small capillaries, with a few larger muscularized feeder vessels, several of which appeared to arise from 1 umbilical artery. Cells showed bland cytologic features with no mitotic figures (Figure 2(c)). Glut-1 immunohistochemical staining was negative in the vascular lesion, with good controls (Figure 2(e)). Cystic changes in the Wharton’s jelly surrounding the tumor and in the separate dilated region of umbilical cord showed myxedematous, paucicellular Wharton’s jelly with cystic regions lacking epithelial or endothelial lining.

Case 4

A 36-year-old G5P2 mother at 37 weeks gestation, complicated by polyhydramnios underwent spontaneous vaginal delivery. The newborn weighed 3080 g. Gross examination revealed a fusiform lesion of the umbilical cord measuring 23 cm × 6.5 cm near the placental insertion site. The lesion was sharply demarcated from the remainder of the umbilical cord, which was normal in caliber, but hypercoiled at 15 coils per 10 cm. Sectioning the fusiform lesion revealed a variegated red-tan cut surface with focal hemorrhage and associated diffuse edema and hemorrhage. Histologically, the lesion was composed of cytologically bland arborizing small capillaries, which appeared to intercalate within the walls of both umbilical arteries as feeder vessels. The lesion was completely distinct from the umbilical vein.

Literature Search and Statistical Analysis

A Pubmed search of the English-language literature using search terms “umbilical cord hemangioma” and “umbilical cord angiomyxoma” yielded 52 additional cases, for which salient clinical and pathologic findings are also summarized with the aforementioned case series in Table 1. For statistical comparison, fetal outcome was divided into 1 group comprised of liveborns without complications and a second group comprised of those with severe complications and/or resultant demise. One pregnancy terminated solely on the basis of elevated serum alphafetoprotein, which was retrospectively presumed due to the hemangioma,⁷ was excluded from the analysis. A second pregnancy terminated for Klippel Trenaunay syndrome,¹⁷ was also excluded from the analysis. A Fisher exact test was used to assess for differences between fetal outcome and lesion location along the umbilical cord (i.e., fetal vs placental end) as well as whether fetal outcome was different if the vascular lesion only involved a single umbilical artery as opposed to other combinations of umbilical vessel involvement. A 2-tailed t-test was used to assess for a difference in fetal outcome with vascular lesion size. Statistical significance was defined as P < .05. Cases missing the aforementioned parameters were excluded from those specific comparisons. Due to small sample size, cases which designated the hemangioma location as the cord “midpoint” (n = 2) were excluded from the lesion location comparison.

Results

Of all combined 56 pregnancies, lesion size ranged from 0.2 to 23.0 cm in maximum dimension. Thirty-three pregnancies (58.9%) resulted in healthy liveborns, 7 (12.5%) resulted in liveborns with severe complications, 14 (25.0%) resulted in intrauterine or neonatal demise, and 2 pregnancies (3.6%) were terminated for an elevated serum alphafetoprotein,⁷ and Klippel Trenaunay syndrome,¹⁷ respectively. Apart from diffuse neonatal hemangiomatosis,²² severe complications in surviving infants were largely due to prematurity and/or fluid overload.

Eighteen (32.1%) lesions were located at the fetal end, 30 (53.6%) were at the placental end, 2 (3.6%) were at the cord midpoint, and 6 (10.7%) did not specify a cord location. Two (3.6%) cases involved all 3 umbilical vessels, 5 (8.9%) involved both umbilical arteries, 15 (26.8%) involved 1 umbilical artery, 2 (3.6%) involved only the umbilical vein, 6 (10.7%) involved an umbilical artery and the umbilical vein, 2 (3.6%) involved the vitelline capillaries, 1 (1.8%) involved the Wharton jelly capillaries, and 23 (41.1%) did not specify which umbilical vessels were involved.

Of the 52 cases included for statistical analysis, there was no significant association between fetal outcome and vascular lesion location (P = .12) or fetal outcome and single umbilical artery involvement versus involvement of other vasculature (P = .29). The mean length of vascular lesions that resulted in healthy liveborns (mean ± standard deviation: 6.1 ± 4.0 cm) did not significantly differ from those resulting in severe fetal complications and/or demise (5.6 ± 5.0 cm; t = 0.36, P = .72). Cases resulting in severe complications and/or demise were significantly earlier in gestation at delivery than those resulting in healthy liveborns (liveborn: 37.2 ± 2.3 weeks; demise: 30.1 ± 7.1 weeks; t = -5.41, P < .001).

Discussion

Although a seemingly simple pathologic diagnosis, umbilical cord hemangiomas are high risk lesions by virtue of their precarious location and potential for catastrophic effects on the developing fetus. This is the first case series of umbilical cord hemangiomas that combines those previously reported in the literature to generate rudimentary data as to which pathologic reporting parameters may be associated with pregnancy outcome. One might assume that a larger lesion would confer a poorer pregnancy prognosis but our analysis showed that the mean size of hemangiomas in pregnancies resulting in severe fetal complications and/or demise did not significantly differ than those resulting in good pregnancy outcome. This finding, combined with the observation that the pregnancies resulting in fetal demise occurred at a significantly lower gestational age, suggests that functional lesion characteristics, such as the degree of turbulent flow generated, have more significance than its size, especially in early gestation losses. That being said, the data may also be confounded by the lack of a standardized method to obtain the lesion size. Some publications specify the size of the hemangioma itself separately from the degree of cystic change, while other publications seem to combine the 2 parameters.

The lack of association between single umbilical artery involvement and better prognosis was unexpected and perhaps reflective of sample size limitations. Twenty-two of the 52 cases reported in the literature did not specify which umbilical vasculature the hemangioma involved. The lack of association between pregnancy outcome and fetal versus placental location was less hampered by sample size. Only 6 previous publications did not report the cord location and 2 reported the cord location as midpoint and were therefore omitted from analysis.

There are occasional cases associated with systemic congenital vascular anomalies such as Klippel Trenaunay syndrome and diffuse neonatal hemangiomatosis. Presence of these systemic congenital vascular anomalies in the developing fetus increase risk for hematologic complications such as localized intravascular coagulopathy.⁵¹ There are no reports of cord hemangiomas in patients with aneuploidy or heritable syndromes.

The purported origins and nomenclature of hemangiomas involving the umbilical cord are not well established. Kaur et al’s³ recent case report suggests that the term “hemangioma” be reserved for lesions representing true infantile hemangiomas based on presence of Glut-1 expression whereas the term “angiomyxoma” should be used in proliferations that are negative Glut-1, therefore implying an origin from remnant vitelline duct vessel remnants within the umbilical cord. This proposed definition is meant to fall in line with previous assertions made for cutaneous vascular anomalies that Glut-1 negative lesions represent vascular malformations as opposed to true neoplastic processes.⁵² We feel without evidence of Wharton jelly contribution to the neoplastic process, use of the term “angiomyxoma” is misleading. That being said, future studies evaluating for a difference in pregnancy prognosis between Glut-1-positive and Glut-1-negative vascular umbilical cord lesions may be of value. Until such data becomes available, the utility of Glut-1 staining in this context remains to be seen.

Moving forward, more robust sample sizes with consistent documentation of pathologic features and fetal outcomes are paramount to progress our understanding of these lesions.

Footnotes

Acknowledgements

The authors would like to thank Dr. Raj Kapur and maternal-fetal medicine specialists Dr. Rachelle Govia and Dr. Jennifer Hunt for their assistance with acquiring cases for this study.

Authors’ Note

One of the cases and preliminary literature review were presented in poster format at the November 2021 Society for Pediatric Pathology fall meeting.

Data Availability Statement

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Elizabeth O Ferreira

References

North

Waner

Mizeracki

, et al A unique microvascular phenotype shared by juvenile hemangiomas and human placenta. Arch Dermatol. 2001;137(5):559.

Iglesias-Deus

Pérez-Muñuzuri

Urisarri

Bautista-Casasnovas

Couce

ML.

Umbilical cord and visceral hemangiomas diagnosed in the neonatal period: a case report and a review of the literature. Medicine (Baltimore). 2016:95:e5196.

Kaur

Heerema-McKenney

Kollikonda

Karnati

Changing course of an umbilical cord mass- chasing the diagnosis of angiomyxoma. Pediatr Dev Pathol. 2022;25:558-561.

Heifetz

Rueda-Pedraza

ME.

Hemangiomas of the umbilical cord. Pediatr Pathol. 1983;1:385-398.

Seifer

Fergusion

2nd Behrens

Zemel

Stevenson

Ross

JC.

Nonimmune hydrops fetalis in association with hemangioma of the umbilical cord. Obstet Gynecol. 1985;66:283-286.

Dombrowski

Budev

Wolfe

Sokol

Perrin

Fetal hemorrhage from umbilical cord hemangioma. Obstet Gynecol. 1987;70:439-442.

Barson

Donnai

Ferguson

, et al Haemangioma of the cord: further cause of raised maternal serum and liquor alpha-fetoprotein. Br Med J. 1980;281:1252.

Armes

Billson

VR.

Umbilical cord hemangioma associated with polyhydramnios, congenital abnormalities and perinatal death in a twin pregnancy. Pathology. 1994;26:218-220.

Sahinoglu

Uludogan

Delikara

NM.

Prenatal sonographic diagnosis of Klippel-Trenaunay-Weber syndrome associated with umbilical cord hemangioma. Am J Perinatol. 2003;20:1-6.

10.

Miller

Gauderer

MW.

Hemangioma of the umbilical cord mimicking an omphalocele. J Pediatr Surg. 1997;32:810–812.

11.

Malliah

Shah

Heller

DS.

Umbilical cord hemangioma associated with multiple cutaneous hemangiomas in a newborn. Int J Gynaecol Obstet. 2007;99:58.

12.

Sathiyathasan

Jeyanthan

Hamid

. Umbilical hemangioma: a case report. Arch Gynecol Obstet. 283(S1):15-17.

13.

Kamitomo

Sueyoshi

Matsukita

Matsuda

Hatae

Ikenoue

Hemangioma of the umbilical cord: stenotic change of the umbilical vessels. Fetal Diagn Ther. 1999;14:328-331.

14.

Daniel-Spiegel

Weiner

Gimburg

Shalev

The association of umbilical cord hemangioma with fetal vascular birthmarks. Prenat Diagn. 2005;25:300-303.

15.

Matsuda

Sato

Marutsuka

Sameshima

, et al Hemangioma of the umblilical cord with pseudocyst. Fetal Pediatr Pathol. 2011;30:16-21.

16.

Lok

Law

Leung

. Prenatal diagnosis of umbilical cord hemangioma. Ultrasound Obstet Gynecol. 2022;59:392-393.

17.

Sun

Chen

Prenatal ultrasound diagnosis of Klippel-Trenaunay-Weber syndrome associated with umbilical cord hemangioma. J Clin Ultrasound. 2021;49:254-256.

18.

Resta

Luthy

Mahony

BS.

Umbilical cord hemangioma associated with extremely high alpha-fetoprotein levels. Obstet Gynecol. 1988;72:488-491.

19.

Cheng

Hsu

Chen

TH.

Angiomyxoma of the umbilical cord. Taiwan J Obstet Gynecol. 2006;45:360-362.

20.

Akiba

Miyakoshi

Ochiai

Kawaida

Matsumoto

Tanaka

Umbilical cord hemangioma: sonographic features by HDlive flow. Eur J Obstet Gynecol Reprod Biol. 2018;221:195-196.

21.

Göksever

Celiloğlu

Küpelioğlu

Angiomyxoma: a rare tumor of the umbilical cord. J Turk Ger Gynecol Assoc. 2010;11:58-60.

22.

Schwickert

Seeger

Pancourt

Henrich

. Prenatally detected umbilical cord tumor as a sign of diffuse neonatal hemangiomatosis. J Clin Ultrasound. 2019;47:366-368.

23.

Ghidini

Romero

Eisen

Smith

Hobbins

JC.

Umbilical cord hemangioma. Prenatal identification and review of the literature. J Ultrasound Med. 1990;9:297-300.

24.

Søndergaard

Hemangioma of the umbilical cord. Acta Obstet Gynecol Scand. 1994;73:434-436.

25.

Vougiouklakis

Mitselou

Zikopoulos

Dallas

Charalabopoulos

Ruptured hemangioma of the umbilical cord and intrauterine fetal death, with review data. Pathol Res Pract. 2006;202:537-540.

26.

Natalucci

Wisser

Weil

, et al Your diagnosis? Umbilical cord tumor. Eur J Pediatr. 2007;166:753–756.

27.

Papadopoulos

Kourea

Adonakis

Decavalas

GO.

A case of umbilical cord hemangioma: Doppler studies and review of the literature. Eur J Obstet Gynecol Reprod Biol. 2009;144:8-14.

28.

Smulian

Sarno

Rochon

Loven

VA.

The natural history of an umbilical cord hemangioma. J Clin Ultrasound. 2016;44:455-458.

29.

Pollack

Bound

LM.

Hemangioma of the umbilical cord. Sonographic appearance. J Ultrasound Med. 1989;8:163-166.

30.

Jacques

Qureshi

Hemangioma of the umbilical cord with amniotic epithelial inclusion cyst. Fetal Pediatr Pathol. 2013;32:235-239.

31.

Weyerts

Jones

Grafe

Scioscia

AL.

Umbilical cord haemangioma associated with an eruptive cutaneous haemangioma in a female infant. Prenat Diagn. 1993;13:61-64.

32.

Yavner

Redline

RW.

Angiomyxoma of the umbilical cord with massive cystic degeneration of Wharton’s jelly. Arch Pathol Lab Med. 1989;113:935-937.

33.

Wilson

Magee

Sorenson

Johnson

In utero decompression of umbilical cord angiomyxoma followed by vaginal delivery. Am J Obstet Gynecol. 1994;171:1383-1385.

34.

Rocha

Rodrigues

Braga

Umbilical cord hemangioma with pseudocyst: an exceptional finding. Acta Med Port. 2017;30:662.

35.

Jakobovits

Herezeg

Haemangioma of the umbilical cord. Ann Chir Gynaecol. 59:159-161, 1970.

36.

Carvounis

Dimmick

Wright

VJ.

Angiomyxoma of umbilical cord. Arch Pathol Lab Med. 1978;102:178-179.

37.

Angelico

Spadola

Ieni

, et al Hemangioma of the umbilical cord with associated amniotic inclusion cyst: two uncommon entities occurring simultaneously. Pathologica. 2019;111:13-17.

38.

Bernischke

Dodds

JP.

Angiomyxoma of the umbilical cord with atrophy of an umbilical artery. Obstet Gynecol. 1967;30:99-102.

39.

Tekant

Kasabaligil

Abbasoglu

Sever

Evren

Bulut

Giant umbilical cord associated with cord hemangiomas. Pediatr Surg Int. 1993;8:82-83.

40.

Tennstedt

Chaoui

Bollmann

Dietel

Angiomyxoma of the umbilical cord in one twin with cystic degeneration of Wharton’s jelly. A case report. Pathol Res Pract. 1998;194:55-58.

41.

Jauniaux

Mascoso

Chitty

Driver

Campbell

An angiomyxoma involving the whole length of the umbilical cord. Prenatal diagnosis by ultrasonography. J Ultrasound Med. 1990;9:419-422.

42.

Iyoob

Tsai

Ruchelli

Coleman

Wilson

RD.

Large umbilical cord hemangioma: sonographic features with surgical pathologic correlation. J Ultrasound Med. 2006;25:1495-1498.

43.

Gramellini

Pedrazzoli

Sacchini

Montalto

Piantelli

Color Doppler ultrasound in prenatal diagnosis of umbilical cord angiomyxoma. Case report. Clin Exp Obstet Gynecol. 1993;20:241-244.

44.

Fortune

Ostor

Angiomyxomas of the umbilical cord. Obstet Gynecol. 1980;55:375-378.

45.

Zhang

Delisle

Hendson

, et al Umbilical cord hemangioma with significant cord edema. J Obstet Gynaecol Can. 2023;45:101785. doi:10.1016/j.jogc.2021.06.012

46.

Barry

McCoy

Callahan

WP.

Hemangioma of the umbilical cord. Am J Obstet Gynecol. 1951;62:675-680.

47.

Gouin

Kingdom

Keating

A giant cord hemangioma diagnosed at 32 weeks’ gestation. J Obstet Gynaecol Can. 2009;31:695.

48.

Mishriki

Vanyshelbaum

Epstein

Blanc

Hemangioma of the umbilical cord. Pediatr Pathol. 1987;7:43-49.

49.

Calderella

Buccoliero

Taddei

Savino

Taddei

GL.

Hemangioma of the umbilical cord: report of a case. Pathol Res Pract. 2003;199:51-55.

50.

Hara

Fukumura

Saito

, et al A giant cord hemangioma with extramedullary hematopoiesis and elevated maternal serum human chorionic gondadotropin: a case report and review of the literature. Diagn Pathol. 2015;10:154.

51.

John

PR.

Klippel-trenaunay syndrome. Tech Vasc Interv Radiol. 2019;22(4):100634.

52.

van Vugt

van der Vleuten

CJM

Flucke

Blokx

WAM.

The utility of GLUT1 as a diagnostic marker in cutaneous vascular anomalies: a review of literature and recommendations for daily practice. Pathol Res Pract. 2017;213:591-597.