|Ahead of print publication
Fetal accessory renal arteries and other renal anomalies
Dinit K Tom, Purushottam Rao Manvikar, Maitreyee Madhav Mutalik
Department of Anatomy, Dr. D. Y. Patil Medical College and Research Center, Pune, Maharashtra, India
|Date of Submission||29-Jan-2021|
|Date of Decision||04-Feb-2021|
|Date of Acceptance||11-Apr-2021|
Dinit K Tom,
Flat No. 203B, Richwoods Housing Society, Spine Road, Pune - 411 019, Maharashtra
Source of Support: None, Conflict of Interest: None
Background: Human kidneys develop from intermediate mesoderm, in three successive stages; pronephros, mesonephros and metanephros. The definitive kidney, which is derived from metanephros occupy sacral region initially, which ascent later, reaching the adult position by 9th week. It receives blood supply from different sources during its development and ascent. Accessory renal arteries are widely studied in adults while the same in fetuses is an understudied topic. Aims and objectives: The present study was carried out to find out the percentage of accessory renal arteries in fetuses and associated positional congenital anomalies with it. Materials and methods: Fifty fetuses of gestational ages ranged from 14 to 40 weeks were collected from the department of Obstetrics and Gynecology, with prior permission from Head of the department and Dean. Results: The study showed a higher percentage of accessory renal arteries in fetuses (30%) and in 2 out of 50 fetuses dissected (4%), accessory renal arteries were found to be associated with positional anomalies. One was a case of bilateral ectopic kidney whereas the other was a horseshoe kidney (HSK). Lobulation were seen in most of the kidneys and 3 cases of bilateral accessory renal arteries without any obvious anomalies were noted. Conclusion: As the advancement in prenatal diagnostic techniques, screening for accessory renal arteries in fetuses can provide a clue for associated congenital renal anomalies. Knowledge on vascular variation in fetuses will help pediatric surgeons in planning abdominal surgeries in new born and children of early ages, where vascular anatomy may be different than in adults.
Keywords: Accessory renal arteries, ectopic kidney, fetal dissection, horseshoe kidney
| Introduction|| |
In human, the definitive metanephric kidney develops in the sacral region. It receives its blood supply from different sources as it ascent to its normal position. This process is accompanied by subsequent sprouting of branches from the abdominal aorta while lower branches disintegrate. This fact accounts for the variations in number, location, and branching pattern of renal arteries. Definitive renal artery represents the lateral splanchnic branch of the aorta at the level of L2.
Variations in the number of renal arteries are common; it is considered as a rule rather than an exception. There are many studies available, describing the different types of variations and their incidences in adults.,, Incidence of accessory renal arteries in the Indian population ranges from 13.3%. to 62.2%. Their frequencies reveal its complexity in organogenesis.
Variations in the location of fetal renal arteries with respect to vertebral level and incidence of multiple renal arteries in fetuses have not been discussed in most of the studies and its a fact that infants are not miniatures of adults in some of the aspects when their vascular anatomy is concerned. Here comes the need of gross anatomical study of fetal vasculature by dissection method as it can provide a better insight into the actual anatomy.
Association between accessory renal arteries and congenital renal malformations has been already reported., There have been numerous studies titles the association between the presence of accessory renal arteries, an increased risk of renal artery stenosis and the development of arterial hypertension later in life. With the evolving technologies in prenatal diagnostics, early detection in variations in renal arteries can be useful for surgical procedures in the abdominal cavity and for screening the severe and difficult to manage hypertension in later life.
The present study aimed at providing insight about variations of renal arteries during intrauterine life which may be supportive in the differential diagnosis of kidney-related clinical scenarios.
| Materials and Methods|| |
Fifty fetuses of gestational ages ranged from 14 to 40 weeks were collected from the Department of Obstetrics and Gynecology, with prior permission from the Head of the department and Dean. Institutional ethical clearance (Ref.No. DYPV/EC/53/16 dated; 24-05-2016) was obtained before the commencement of the study and written informed consents were taken from the parents of fetuses. Fetuses were divided into four groups based on their gestational age as given in [Table 1]. The anterior abdominal wall was reflected laterally by putting incisions along A. Midline B. Along the coastal margin, C. Along inguinal ligament [Figure 1]. The peritoneum and coils of intestines were removed to expose the kidney. Renal arteries were dissected carefully and veins were removed for better clearance. Necessary photographs were taken for the assessment and demonstration of variations.
|Figure 1: Skin incision on the anterior abdominal wall: A. Midline B. Along the costal margin, C. Along inguinal ligament|
Click here to view
| Results|| |
Accessory renal arteries
Accessory renal arteries were observed in 30% cases. Different types of accessory arteries observed in the study and their percentages are shown in [chart 1].Among these accessory arteries, all were the branches of the abdominal aorta except one, where the left accessory renal artery originated from the superior mesenteric artery.
Double renal arteries were noted in 28% of cases while triple renal arteries were observed on the left side of two fetuses (2%).
Most of the kidneys appeared lobulated without any obvious anomalies. These were not considered as variations as the fetal kidneys show lobulation during the period of development.
Bilateral accessory renal arteries
Bilateral accessory arteries were observed in 3 cases (6%).
In this case, the right showed an upper polar accessory renal artery originated from the abdominal aorta 1 cm above the origin of the main renal artery, while on the left side, accessory renal artery arose from the abdominal aorta just below the origin of the main renal artery [Figure 2].
|Figure 2: Bilateral accessory renal artery case I. Right superior polar and left hilar accessory renal arteries. RRA: Right renal artery, RARA: Right accessory renal artery, LRA: Left renal artery, LARA: Left accessory renal artery|
Click here to view
In this case of the bilateral accessory renal artery, the right side showed two renal arteries and the left side showed three renal arteries. On the right side, the main renal artery originated from the abdominal aorta at the level of L1, passed downward and laterally, and divided into segmental branches before entering the hilum and accessory renal artery (right accessory renal artery) originated from the abdominal aorta at the level of the disc between L2/L3 [Figure 3].
|Figure 3: Bilateral accessory renal artery case II right hilar accessory renal artery and left hilar and inferior polar accessory renal arteries. RRA: Right renal artery, RARA: Right accessory renal artery, LRA: Left renal artery, LARA: Left accessory renal artery|
Click here to view
On the left side, all three renal arteries originated from the abdominal aorta, at the levels of the upper border of L1, the middle part of L1, and the disc between L2/L3 from above downward. The 3rd one was found to be an inferior polar artery which crossed the ureter anteriorly.
In this case of the bilateral accessory renal artery, the right main renal artery originated from the lateral part of the abdominal aorta at the level of L2 and the inferior polar accessory renal artery arose from the anterior aspect of the abdominal aorta at the level of L3 along with the origin of the inferior mesenteric artery. The left side showed three renal arteries. The main left renal artery originated bit higher than the right renal artery, upper accessory renal artery, took origin from the superior mesenteric artery, passed downward to enter the hilum. It showed prehilar divisions. The second accessory renal artery originated from the abdominal aorta at the level of L3 which was seemed to be an inferior polar artery [Figure 4].
|Figure 4: Bilateral accessory renal artery case III. Right hilar accessory renal artery and left hilar and lower polar accessory renal arteries. RRA: Right renal artery, RARA: Right accessory renal artery, LRA: Left renal artery, LARA: Left accessory renal artery, SMA: Superior mesenteric artery|
Click here to view
Horse Shoe Kidney
In one of the fetuses (GA-25 weeks), Horseshoe Shaped Kidney has been observed. The lower poles of both the kidneys were fused at the isthmus. Isthmus was crossed anteriorly by inferior mesenteric vessels; thus, the ascent was found to be arrested. Both hila faced anteriorly and ureters crossed the corresponding side kidneys anteriorly. The upper pole of the right kidney (L3) being placed at lower than the left kidney (L2), lower poles of both kidneys and isthmus were at the level of L5 vertebrae [Figure 5].
Blood supply of horseshoe kidney
Horseshoe kidney (HSK) was supplied by three arteries; one on the right side which took origin from the aorta at the level of L3 vertebrae, whereas the left side showed two renal arteries; upper one was at the level of L1 and an inferior accessory renal artery originated at the level of L2.
Bilateral ectopic kidney
Bilateral ectopic kidney was observed in one of the fetuses studied (GA-24 weeks). In this case; both the kidneys were placed below the level of L2 vertebrae. The superior pole lied at the level of L3 and the inferior pole of the right kidney rested on the iliac crest. The superior pole of the left kidney was found to be situated at the level of L2 and the inferior pole was at the level of L4. Both kidneys appeared nonlobulated [Figure 6].
|Figure 6: Bilateral ectopic kidneys: Both kidneys are in lower lumbar region. RK-Right kidney, LK-Left kidney, RRA1-Right renal artery 1, RRA2-Right renal artery 2, LRA-Left renal artery|
Click here to view
Blood supply to ectopic kidney
The right kidney was supplied by two renal arteries; both originated from the anterior aspect of the abdominal aorta rather than its lateral aspect. The upper one took origin from the aorta at the level of L1 while the lower one originated at the level of L2 vertebrae. The left kidney was supplied by single renal artery, which originated from the abdominal aorta at the level of L1. All the three arteries entered the kidneys through its upper pole rather than the hilum.
| Discussion|| |
Study on variations in the renal arteries is important, as this is a region where arterial variations are more common than venous variations, in contrast to other regions, where variations in veins are more common. Change in position of kidney in fetal life accounts for its differences in blood supply and high occurrence of accessory renal arteries. Aberrant arteries were recorded for the first time by Eustachius in 1552. The incidence of accessory renal arteries in the Indian population ranges from 13.3% to 62.2%. However, there are very less descriptions about multiple renal arteries in fetuses in the literature and there is hardly any studies describing variations in the number of renal arteries and the percentage of occurrence of multiple renal arteries in fetuses of the Indian population.
Incidences of multiple renal arteries in fetuses, observed by different authors in other populations are 13% and 25% The present study reports a higher percentage (30%) of occurrences of accessory renal arteries in fetuses of the Indian population.
Accessory renal arteries are categorized depending on their mode of entry into the renal parenchyma as hilar (both arteries enter via hilum), upper polar or lower polar. In the present study, 14% of accessory renal arteries were hilar, 5% were superior polar arteries, whereas 11% were inferior polar arteries. Ciçekcibaşi et al. reported 11.1% hilar, 3.3% superior polar, and 10.5% inferior polar arteries in fetuses.
Patil and Shirshirkumar found 4% of hilar, 4% of superior polar, and 20% inferior polar accessory arteries in a cadaveric study. Most of the studies, including the present study, reported more incidence of inferior polar arteries than superior polar arteries. In some of the reports, incidences of superior polar arteries were more than inferior polar arteries., Comparison of the percentage of various types of accessory renal arteries observed in different studies and present study is shown in [Table 2].
|Table 2: Comparing the percentage of various types of accessory renal arteries observed in different studies and present study|
Click here to view
Wadha reported 1%–2% incidence of triple renal arteries in a cadaveric study. They observed triple renal arteries on the right side and double renal arteries on the left side. Jamkar et al. observed 3.77% of triple renal arteries on the left side, 4.71% on the right side. Mahalakshmi et al. reported 3 cases (6%) of triple renal arteries; two on the right side and one on the left side out of 50 kidneys. The present study noted triple renal arteries only on the left side of two fetuses (4%). Mustafa et al. in a study of 549 kidneys by different methods; like dissection, postmortem, and angiography 2% of triple renal arteries on the right side and 2.73% in the left side were observed.
Bilateral accessory renal arteries
In the present study, the frequency of bilateral accessory renal artery was 6%. This was found to be similar to the findings of Aragão et al., Ciçekcibaşi et al., Syamala et al. and Ozkan et al. who found frequencies of, 3.3%, 7.7%, 6%, and 5%, respectively. Differing from the reports by Harrison et al. where they found only 2.4% of bilateral accessory renal arteries in a renal arteriographic study on 166 kidneys.
Palmieri et al. reported the highest frequency of bilateral multiple renal arteries (41%) in 200 renal pedicles. Among these multiple renal arteries, 75% on right and 62.7% on left had their origin as a division of primary prehilar arteries from the main renal artery. 10.7% on the right and 23.9% on the left had aortic origin, 14.3% and 13.4% (on right and left, respectively) had one or more arteries from the aorta, in addition to prehilar branches from the main artery. This high percentage of incidence maybe because prehilar divisions of renal arteries were included under multiple renal arteries in this study.
Accessory renal arteries may originate from the abdominal aorta, renal arteries, and rarely from the testicular artery. The present study reported the origin of the upper accessory renal artery from the superior mesenteric artery on the left side in one of the fetuses, which entered renal parenchyma through the hilum. A similar case was reported by Kommuru et al., in a study on accessory renal arteries in 92 cadavers.
Any injury to SMA can leads to ischemic bowel and if an accessory renal artery originating from SMA is left unnoticed, it may damage that particular segment of the kidney supplied by it; as these arteries are believed to be the end arteries.
HSK is a positional anomaly, believed to befall during 4–6 weeks of development where lower poles of both the kidneys are fused. It lies in the hypogastrium, anterior to the aorta and lower lumbar vertebra. Ascent of the kidney is prevented by an inferior mesenteric artery which crosses the isthmus of HSK anteriorly. It occurs in one in 400 of births.
One case of HSK was detected out of 50 fetuses (2%). Even though it is said to be an asymptomatic renal anomaly, Scott J E S reported 57.7% (323 cases) of death in fetuses (221 prenatal deaths) and babies (102 postnatal deaths) exclusively due to anomalies of the urinary system; the commonest being HSK. And the author also reported that in 42.4% of chromosomal anomalies were associated with HSK. There have been numerous reports on the association of HSK with fetal syndromes such as Turner syndrome (7%), trisomy 18, and trisomy 9.,
Detection of HSKs by prenatal diagnostic techniques is comparatively difficult because of echogenicity of renal parenchyma with respect to bowels as a result of relatively lower position. Children with HSK are 2–8 times more prone to develop Wilm's tumor. Regardless of the advances in imaging techniques, the presence of Wilm's tumor associated with HSK went unnoticed preoperatively in 13 out of 41 patients.
Singh et al. proposed that sagging renal arteries can be used as a clue for prenatal detection of HSKs in fetuses. The findings of the present study support this suggestion, as the same was observed regarding the renal arteries supplying HSK. In the present case of HSK, there were two renal arteries on the left side, originated at the levels of L1 and L2 and moved downward to supply the incompletely ascended HSK. On the right side, the renal artery had an oblique course though it was a single renal artery.
However, early detection of this anomaly is important as it may be associated with other congenital anomalies hence can help in the diagnosis and management of associated anomalies. It is essential to seek out for chromosomal anomalies in suspected case of HSK.
Bilateral ectopic kidneys
Lumbar ectopic kidneys are placed above the iliac crest but below the level of L2 and L3. Incidence of the ectopic kidney is 1:900, being bilateral in 10% of cases; most of the ectopic kidneys are functional and show lobulation. In the present case, it looked nonlobulated and the hilum was not conspicuous. It received blood supply from the abdominal aorta and right side showed accessory renal artery. Arteries arose at the level of L1 and L2 and passed obliquely downwards to supply the ectopic kidneys. There have been reports on ectopic pelvic kidneys with accessory renal arteries linked with renovascular hypertension in children.
With the advancement in prenatal diagnostic techniques, early detection of the ectopic kidney is now possible. Even though, some factors like the larger size of suprarenal gland, fetal bowel in renal fossa, or lack of normal echogenicity by fat surrounding the kidney may make the identification of fetal kidney bit difficult for radiologists,, early detection of such anomalies are important as it can be associated with other congenital anomalies of cardiovascular, reproductive or skeletal systems too. Color Doppler is found to have more advantage in identification of these anomalies; better identified in the late second trimester to early 3rd trimester. Prenatal recognition of such anomalies enables in reduction of morbidity due to unnoticed ectopic kidneys and will help in parental counseling., Peoples with such types of anomalies should be advised to avoid participation in contact sports as pelvic kidneys are more vulnerable to injuries since they are not protected by the rib cage. Timely detection and application of suitable treatment at the earliest can prevent the infection of the kidney and permanent damage to renal parenchyma.
In the present study, congenital anomalies were observed in 2 of 50 fetuses (4%). One was a bilateral ectopic kidney and the other was a HSK. Reddy in a study of 50 embalmed fetuses reported the same percentage (4%) of congenital anomalies; one being unilateral renal agenesis and the other; a polycystic kidney.
Other congenital anomalies such as renal agenesis, abnormal rotation, and double ureter were not observed in this study.
| Conclusion|| |
The present study investigated the percentage of accessory renal arteries and its association with congenital anomalies in fetuses by dissection method. Knowledge on these types of variations in fetuses helps to avoid complications during prenatal investigations and antenatal vascular surgeries of the abdomen. Our observations may be of help in prenatal and preoperative diagnosis and when there is a need for spectral Doppler sampling from renal arterial trunk or ramifications.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Sadler TW. Langman's Medical Embryology.12th ed. Philadelphia: Lippincott Williams and Wilkins; 2012. p. 233
William P.L, Bannister L.H ,Berry M.M.Collins Gray's Anatomy. 38edi. Newyork:Churchill Livingstone;1995:1815-1828.
Cases C, García-Zoghby L, Manzorro P, Valderrama-Canales F J, Munoz M, et al
. Anatomical variations of the renal arteries: Cadaveric and radiologic study, review of the literature, and proposal of a new classification of clinical interest. Ann Anat. 2017; 211: 61-68.
Gulas E, Wysiadecki G, Szymański J, Majos A, Stefańczyk L, Topol M, et al
. Morphological and clinical aspects of the occurrenceof accessory (multiple) renal arteries. Arch Med Sci.2018;14(2):442–453.
Budhiraja V, Rastogi R, Ajankar V, Ramesh Babu C S, Goel P. Supernumerary renal arteries and their embryological and clinical correlations: A cadaveric study from north India.;ISRN Anatomy. 2013; 2013:1-4. http://dx.doi.org/10.5402/2013/405712
Aristotle S, Sundarapandian, Felicia C. Anatomical study of variations in the blood supply of kidneys. Journal of Clinical and Diagnostic Research.2013; 7(8): 1555-1557.
Degani S, Leibovitz Z, Shapiro I, Ohel G. Variations of the origin of renal arteries in the fetus identified on power dopplerand 3d sonography. Journal Of Clinical Ultrasound.2010; 38(2):59-65.
Sasikala P, Sulochana S, Rajan T, Mohan J, Rajendran S M. Comparative study of anatomy of renal artery in correlation with the computed tomography angiogram. World J. Med. Sci.2013;8 (3) : 300-305.
Priestman W S, DeNunzio M, Taal M W, Fluck RJ, McIntyre C W. An unusual case of renovascular hypertension–Renal artery stenosis. Nephrol Dial Transplant.2005; 20 :2861-2863
Hollinshead W H. Anatomy for sugeons.The thorax abdomen and pelvis.Vol. 2.2edi:London; Harper and Row.1982:518-560.
Graves F T. The aberrant renal artery. J Of Anat.1956; 90:553-558.
Aragao J A, de Oliveira Pacheco J M, Silva L A, Reis F P. Frequency of multiple renal arteries in human fetuses. Surg Radiol Anat.2012; 34:133–136.
Cicekcibasi A E, Ziylan T, Salbacak A, Seker M, Buyumumcu M, Tuncer I. An investigation of the origin, location and variations of the renal arteries in human fetusesand their clinical relevance. Ann Anat.2005; 187: 421—427.
Patil G V, Shirshirkumar. (2014). Study on aberrant renal arteries in south indian polpulation. International Journal of Science and Research.2014; 3(8):1-3.
Petru B, Elena S, Dan I, Constantin D. The morphology and the surgical importance of the gonadal arteries originating from renal artery. Surgical and Radiologic Anatomy. 2007;29(5):367-371.
Saldarriaga B, Perez AF, Ballesteros LE. A direct anatomical study of additional renal arteries in a Colombian mestizo population. Folia Morphol.2008; 67(2): 129–134.
Mahalakshmi R, Dinesh Kumar D, Ratna Kumari K, Bala Sekharan C. Morphological study of renal arteries in south Indian population. Saudi Journal of Medicine.2016; 1(3): 76-81.
Kommuru H, Sreelekha D, Jothi SS, Rajeswararao N, Sujatha N. Presence of renal artery variations and its surgical correlation. International Journal Of Medical And Clinical Research.2012;3(5): 176-179.
Vatsala AR, Ajay KT, Mavishettar GF, Sangam. A study on branching pattern of renal arteries. Int J Anat Res.2014, vol 2(1):270-72.
Wadha SS. A.Multiple variations in the paired arteries of abdominal aorta –Clinical implications. Journal of Clinical and Diagnostic Research.2010;4:2622-2625.
Jamkar AA, Khan B, Joshi DS. Anatomical study of renal and accessory renal arteries. Saudi J Kidney Dis Transpl 2017;28(2):292-297.
Mustafa AYAE, Mohammed Ali Q, Elimam MQ. Presence of accessory renal artery in Sudanese people. International Journal of Anatomy and Research.2016; 4(1):1931-40.
Syamala G, Balla LM, Prasad KSN. Morphology and variations of renal artery pattern: A case report. IOSR Journal of Dental and Medical Sciences.2015; 14(4):29-31.
Ozkan U, Oğuzkurt L, Tercan F, Kızılkılıç O, Koç Z, Koca N.Renal artery origins and variations: angiographic evaluation of 855 consecutive patients. Diagn Interv Radiol.2006;12 :183-186.
Harrison LH, Flye MW, Seigler HF. Incidence of anatomical variants in renal vasculature in the presence of normal renal function. Ann. Surg.1978;188(1):83-89.
Palmieri BJ, Petroianu A, Silva LC, Andrade LM, Alberti LR. Study of the arterial pattern of 200 renal pedicles through angiotomography. Rev Col Bras Cir. 2011; 38(2):116-121.
Mao QH, Li J. An accessory renal artery originating from the testicularartery, A rare variant. Indian J Surg.2015;77(6): 549–550.
Bamac B, Colak T, Ozbek A, Gundogmus U N. A report of unusual origin of right renal artery. International Journal of Anatomical Variations .2011; 4:95–97.
Skandalakis JE. Skandalakis' Surgical Anatomy. The embryologic and Anatomic basis of modern surgery.Vol.2. Paschalidis Medical Publication ltd. International Student Edition. Greece.2004.1297
Holcomb GW, Murphy JP,Ostlie DJ. Ashcraft's Pediatric Surgery. 6edi. London:Saunders elsevier;2014:712-713.
Scott JES . Fetal, perinatal, and infant death with congenital renal anomali. Arch Dis Child 2002;87:114–117.
Coran AG, Adzick NS, Krummel TM, Laberge J, Shamberger RC, Caldamone AA. Paediatric Surgery. Vol. 2 .7edi.Philadelphia: Elsevier Saunders;2012:1403-1408.
Cho JY, Lee YH, Toi A, Macdonald B. (2005). Prenatal diagnosis of horseshoe kidney by measurement of the renal pelvic angle. Ultrasound Obstet Gynecol. 2005; 25(6): 554-8. doi: 10.1002/uog.1904.
Singh D, Kaur L, Sharma A. Sagging renal artery: Clue to prenatal diagnosis of horseshoe kidney. Ultrasound in Obstetrics & Gynecology. 2017; 50 (1): 295.https://doi.org/10.1002/uog.18447
Gutierrez DM, Rodriguez F, Guerra JC. Renal anomalies of position, shape and fusion: radiographic analysis. Revista de la Federación Ecuatoriana de Radiología.2013;6:24-30.
Rouse GA, Kaminsky CK, Saati HP, Grube GL, Fritzsche PJ. Current concepts in sonographic diagnosis of fetal renal disease. RadioGraphics.1988; 8(1):119-132.
Bowie JD, Rosenberg ER, Andreotti RF, Fields SI. The changing sonographic appearance of fetal kidneys during pregnancy.J Ultrasound Med.1983; 2: 505-507.
Dogan CS, Dorterler ME, Aybar MD, Ciftci H, Gulum M, Akin Y, et al
. Associated anomalies and clinical outcome in children with ectopic kidney. Saudi J Kidney Dis Transpl. 2017;28(2):330-335.
Meizner I, Yitzhak M, Levi A, Barki Y, Barnhard Y, Glizerman M. Fetal pelvic kidney:A challenge in prenatal diagnosis?.Ultrasound in Obstetrics and Gynecology.1995;5:391-393.
Reddy PR. Congenital renal abnormalities in fetuses: a study in a teaching institute. Indian Journal of Clinical Anatomy and Physiology.2017;4(4): 465-467.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
[Table 1], [Table 2]