Associations between kidney position and surplus renal arteries in horseshoe kidney: case report and analysis
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1 Okajimas Folia Anat. Jpn., 89(1): 7 13, May, 2012 Associations between kidney position and surplus renal arteries in horseshoe kidney: case report and analysis By Hirokazu NARITA 1 3, Toshiki TANI 1,3 and Yoshikazu TONOSAKI 1 1 Departments of Anatomical Science, Hirosaki University Graduate School of Medicine, Hirosaki, Japan (address: 5 Zaifucho, Hirosaki, Aomori , Japan) 2 Division of Health Sciences, Hirosaki University Graduate School of Health Sciences, Hirosaki, Japan (address: 66-1 Honcho, Hirosaki, Aomori , Japan) 3 These authors contributed equally to this work Received for Publication, March 7, 2012 Key Words: horseshoe kidney; anomaly; gross anatomy Abstract: We report the anatomical findings of a case of horseshoe kidney, and analyze the associations between kidney position and surplus renal arteries in horseshoe kidneys found in Japanese autopsies in the past. The horseshoe kidney of our case fused at the lower poles of the original kidneys. Its right and left upper poles were at the middle region of the first and second lumbar vertebrae, respectively. The kidney was supplied by eight arteries. Our analysis of the correlation between the ascent of a horseshoe kidney and the number of surplus arteries found no significant association. However, there was a significant association between the region of the kidney where the surplus arteries entered and the location where they diverged from the aorta. Therefore, the ascent of a horseshoe kidney is not necessarily arrested because of the existence of many surplus arteries. After a horseshoe kidney partially ascends, the arteries which might become normal renal arteries are generated. In our case, we observed large splenomegaly, and noted that the left upper pole was the lowest compared with the horseshoe kidneys in the past autopsy reports. We suggest it is necessary to consider additional influences that determine the position of a horseshoe kidney. Introduction Horseshoe kidney is one of the most common congenital fusion anomalies of the kidney. The anomaly consists of two distinct renal masses lying vertically on either side of midline and connected at their respective lower or upper poles, presenting a horseshoe shape. Ninety-five percent of horseshoe kidneys are fused at the lower poles. 1) The incidence of horseshoe kidney noted in Japanese reports 2) and in foreign reports 1,3) is 0.15% 0.48% and approximately 0.25%, respectively. The frequency in males is two to three times as high as in females. 1,3) Clinically, many cases of horseshoe kidney produce no symptoms. However, it is reported that persons with horseshoe kidney are more prone to developing infection, hydronephrosis, urolithiasis and ureteropelvic junction obstruction due to the influence of the abnormal ureteral course, the abnormal vessels supplying the horseshoe kidney, and the abnormal motility of the ureteropelvic junction segment. 1,4) During a routine dissection at our institution, we encountered a case of horseshoe kidney in an 83-year-old Japanese male cadaver who died of myocardial infarction. First, we report the anatomical findings of this horseshoe kidney to serve as reference data on this type of anomaly. Then, we analyze the positions of horseshoe kidneys and their surplus arteries found in Japanese autopsies in the past and discuss the distribution pattern of surplus arteries, focusing on the ascent of the horseshoe kidney and factors that prevent its ascent. Case Report 1. Shape, size and position of the kidney In this horseshoe kidney, the fusion of the left and right kidneys at their lower poles formed the isthmus, which was located at the ventral side of the inferior vena cava (Fig. 1). The longitudinal axis of each kidney was directed from the superolateral toward the inferomedial. The border between the isthmus and each kidney was unclear. The right kidney had its upper pole at the level of the middle region of the first lumbar vertebra, and the Correspondence to: Hirokazu Narita, Division of Health Sciences, Hirosaki University Graduate School of Health Sciences, 66-1 Honcho, Hirosaki, Aomori , Japan, phone/fax number: , narihiro@cc.hirosaki-u.ac.jp
2 8 H. Narita et al. Fig. 1. A photograph of the horseshoe kidney and its surroundings, as viewed from the ventral side. RK, right kidney; LK, left kidney; AA, abdominal aorta; CT, coeliac trunk; SM, superior mesenteric artery; IM, inferior mesenteric artery; IVC, inferior vena cava; U, ureter. longitudinal length was approximately 11.7 cm (Fig. 2). The left kidney had its upper pole at the level of the middle region of the second lumbar vertebra, and the longitudinal length was approximately 10.7 cm. The lowest part of the horseshoe kidney was constituted by the lower pole of the left kidney and was at the level of the bottom of the fourth lumbar vertebra. As a whole, it was situated slightly to the right side of the posterior abdominal wall. The right kidney measured 5.5 cm in maximal width and 4.2 cm in maximal thickness. The left kidney measured 5.0 cm in maximal width and 3.3 cm in maximal thickness. The isthmus measured 5.6 cm in maximal width and 2.0 cm in maximal thickness. 2. Renal hila, pelvises and ureters The hilum of each kidney opened widely in the ventral direction. The left renal hilum was larger than that of the right and extended to the vicinity of the bottom region of the horseshoe kidney. The left hilum measured 7.8 cm in longitudinal length and 3.2 cm in maximal width (Fig. 2). The right hilum measured 7.1 cm in longitudinal length and 2.7 cm in maximal width. The pelvis of each kidney was exposed from the hilum. The left and right pelvis each consisted of 4 major calyces. Both ureters originated independently from each side of the pelvis and descended to form a shallow groove on the ventral surface of the kidney. 3. Blood vessels This horseshoe kidney had eight arteries (A1 to A8), which included six surplus arteries (A3 to A8) (Fig. 3). A1 and A2, which correspond to the right and left renal artery in a normal kidney, arose from the abdominal aorta approximately 2 cm below the origin of the superior mesenteric artery. After running dorsal to the inferior vena cava, A1 divided into 2 branches and supplied the upper and posterior region of the right kidney. A2, which ran behind V4, divided into 3 branches and was distributed from the
3 A case report and analysis of position and arteries in horseshoe kidney 9 Fig. 2. Measurements of the horseshoe kidney. upper part of the posterior region to the middle part of the anterior region of the left kidney. A3 arose from the aorta slightly below A1, ran ventral to the inferior vena cava and supplied the middle region of the right kidney. Four surplus arteries (A4 to A7) arose directly from the aorta below the origin of the inferior mesenteric artery. A4 arose from the right side of the aorta 2.2 cm below the origin of the inferior mesenteric artery and entered directly into the inferomedial part of the posterior region of the right kidney. A5, which arose from the ventral side of the aorta 2.7 cm below A4, ascended behind the left kidney and entered directly into the posterosuperior part of it. A6 arose from the right side of the aorta slightly below the origin of A5. After running behind the isthmus to the right, A6 divided into two branches. The right branch immediately entered directly into the lower part of the right kidney. The left branch came around the ventral side and entered into the lower part of the right kidney from the right hilum. A7, which arose from the bifurcation of the right and left common iliac arteries, ascended in front of the aorta and directly supplied the posteroinferior part of the left kidney. We could not find the medial sacral artery in normal position. A8 arose from the left common iliac artery, ran upward, and distributed in the anteroinferior region of the left kidney. The inferior mesenteric artery descended in front of the left kidney with a shallow groove on its surface. This horseshoe kidney had four veins (V1 to V4). The right renal veins (V1 to V3) emerged from the right hilum and opened independently into the inferior vena cava. After emerging from the left hilum, V4 communicated with the left testicular vein and the left suprarenal vein and opened into the inferior vena cava. 4. Other We found large splenomegaly. Analysis of Kidney Position and Surplus Arteries We analyzed the position of horseshoe kidneys and surplus arteries found in Japanese autopsies in the past. The subjects were 18 cases which included 17 cases found in original articles and case reports since ) (which were searched using Ichushi web Ver. 5 (Japana Centra Revuo Medicina) and PubMed) and the present case (Table 1). Table 1 shows the position of the upper pole of each side of the horseshoe kidney, the position of the lower end, and the number of surplus arteries. Because each report noted the kidney position differently, we defined the positions as follows: between vertebrae, upper part of vertebra, middle part of vertebra, and lower part of vertebra.
4 10 H. Narita et al. Fig. 3. A schematic drawing of the horseshoe kidney and its surroundings, as viewed from the ventral side. This shows eight arteries (A1 A8) and four veins (V1 V4). AA, abdominal aorta; CT, coeliac trunk; SM, superior mesenteric artery; IM, inferior mesenteric artery; IVC, inferior vena cava; RC, right common iliac artery; LC, left common iliac artery; U, ureter. 1. The position of the upper pole of a horseshoe kidney In a normal kidney, the position of the right kidney is typically lower than that of the left kidney because of the presence of the liver. In a horseshoe kidney, it is thought that the isthmus prevents its ascent. In order to examine the right-left difference in the position of the upper poles of the horseshoe kidney, we used the Wilcoxon signed rank test to compare the positions of the right upper poles with that of the left upper poles in the 14 out of the 18 study cases where the position of the upper pole of each side was available (marked with # in Table 1A). The statistical significance level was chosen as Statistical analyses were performed with the software package SPSS version 16.0J for Windows (IBM Japan, Ltd., Tokyo, Japan). We found no significant difference between the positions of the right upper poles and the left upper poles in the 14 cases. 2. Surplus arteries In the process of ascent of the kidney during development in the womb, the blood supply continuously changes with the generation of new arteries and degeneration of old arteries. 19) To clarify the association between the degree of ascent and the number of surplus arteries in the 15 out of the 18
5 A case report and analysis of position and arteries in horseshoe kidney 11 Table 1. Kidney position and the number of surplus arteries A. Comparison between the right upper pole and the left upper pole position B. Association between the position of the lower end and the number of surplus arteries Position of the upper pole Position of the lower pole Number of surplus Right left arteries Number of surplus arteries arising from the aorta or common iliac artery below the upper end of the isthmus Present case middle part of L1 middle part of L2 # lower part of L4 # 6 5 Ueyama, et al. 5) upper part of L2 lower part of L1 # upper part of L4 # 3 1 Yakeishi, et al. 6) between L1 and L2 between L1 and L2 # between L4 and L5 # 4 0 Nakamura, et al. 7) upper part of L1 middle part of L1 # lower part of L4 # 2 1 upper part of L1 middle part of L1 # middle part of L5 # 4 3 Yoshinaga, et al. 8) lower part of L1 L3 (lesion) upper part of L5 # 2 0 Chen, et al. 9) lower part of L1 upper part of L1 # lower part of L4 # 4 3 Aida, et al. 10) lower part of L1 upper part of L1 # lower part of L4 # 3 2 Shoumura, et al. 11) lower part of L2 upper part of L2 # between L4 and L5 # 1 0 upper part of L1 upper part of L1 # middle part of L5 # 5 4 Konishi, et al. 12) between L1 and L2 middle part of L1 # between L4 and L5 # 3 1 Kosugi, et al. 13) middle part of L2 upper part of L2 # upper part of L5 # 6 5 Nagashima, et al. 14) middle part of L1 upper part of L1 # no description 5 4 Sekine, et al. 15) lower part of Th12 middle part of Th12 # middle part of L4 # 1 1 Inoue, et al. 16) middle part of L1 upper part of L2 # upper part of L5 # 6 2 Isomura, et al. 17) 40 mm below left kidney upper part of L2 lower part of L4 # mm below left kidney 15 mm above upper no description 1 0 part of L1 Ohkubo, et al. 18) L2 L2 L4 5 4 A. There was no significant difference between the positions of the right upper poles and the left upper poles in the 14 cases (marked with #), using the Wilcoxon signed rank test. B. There was no significant correlation between the position of the lower end of the horseshoe kidneys and the number of surplus arteries in the 15 cases (marked with #), using Spearman s rank correlation coefficient. study cases where the position of the lower pole was available (marked with # in Table 1B), we used Spearman s rank correlation coefficient to calculate the correlation between the position of the lower end and the number of surplus arteries. Furthermore we calculated the correlation between the position of the lower end of the horseshoe kidneys and the number of surplus arteries that arose from the aorta or common iliac artery below the upper end of the isthmus. These were thought to more strongly prevent the ascent of a horseshoe kidney, because after arising from the aorta or common iliac artery, most of these surplus arteries ran toward the right above or obliquely upward. The statistical significance level and software were the same as above. Our analysis showed no significant correlation between the position of the lower end of the horseshoe kidneys and the number of surplus arteries. We also found no significant correlation between the position of the lower end of the horseshoe kidneys and the number of surplus arteries that arose from the aorta or common iliac artery below the upper end of the isthmus. Therefore, we could not find any association between the degree of ascent of the horseshoe kidneys and the number of surplus arteries. Additionally, to clarify the association between the region of the kidney where the surplus arteries entered and the location where the surplus arteries diverged from the aorta or common iliac artery, we divided all the arteries (63 arteries in 18 cases) into two groups. One group included the arteries that arose from the aorta above the upper end of the isthmus (A group). The other group included the arteries that arose from the aorta or common iliac artery below the upper end of the isthmus (B group). We used the Chi-square test to examine the association of the surplus arteries of each group entering directly into the isthmus or into the right or left kidney (Table 2). The statistical significance level and software were the same as above. The results showed significant associations as follows: the surplus arteries that arose from the aorta above the upper end of the isthmus more often entered into the right or left kidney, and the surplus arteries that entered into the isthmus more often arose from the aorta or common iliac
6 12 H. Narita et al. Table 2. Association between the regions of the kidney where surplus arteries entered and the locations where they diverged Arising from the aorta above the upper end of the isthmus (A group) Arising from the aorta or common iliac artery below the upper end of the isthmus (B group) artery below the upper end of the isthmus (χ 2 = , φ = 0.414, p < 0.01). Discussion Entering into right or left kidney Entering into isthmus There were significant associations in the 63 arteries in the 18 cases (p < 0.01), using the Chi-square test, as follows: A group more often entered into the right or left kidney, and the surplus arteries that entered into the isthmus were more often included in B group. The present study detailed the gross anatomical findings at autopsy of a case of horseshoe kidney and analyzed the position of horseshoe kidneys with respect to surplus arteries found in Japanese autopsies in the past. Previous studies of horseshoe kidney have reported its morphological characteristics as follows: 1) a lower position than usual, 2) an open and ventrally facing hilum, 3) passage of the ureter on the ventral surface of the kidney, and 4) the presence of surplus blood vessels. 5,7,8,12,13,15) In the horseshoe kidney of our case, the positions of the right and left upper poles were at the middle regions of the first and second lumbar vertebrae, respectively, and lower than that of a normal kidney. 20) The hila of this horseshoe kidney opened widely in the ventral direction and the ureters descended on its ventral surface. Furthermore, the kidney had many surplus blood vessels: eight arteries and four veins. Therefore, the present horseshoe kidney corresponded with the characteristics of horseshoe kidneys reported by previous studies. In a normal kidney, the upper pole of the right kidney is generally located at the level of the twelfth thoracic vertebra, and half or one vertebra lower than that of the left kidney because of the presence of the liver. However, our analysis showed no significant difference between the positions of both upper poles of horseshoe kidneys. Because the poles of horseshoe kidneys were lower than that of a normal kidney, we inferred that the final position of a horseshoe kidney was decided by a factor other than the liver. In regard to the position of a horseshoe kidney being lower than that of normal kidneys, many previous studies have reported that arrest of ascent is caused by the inferior mesenteric artery pressing on the isthmus, 7,21,22) by the surplus arteries remaining, 8,9,21,22) and by the elongation of the aorta to the caudalis. 5) In our case, because the inferior mesenteric artery descended in front of the left kidney with a shallow groove on its surface, we thought this greatly influenced the interference with the ascent of this horseshoe kidney. Moreover, this horseshoe kidney had many surplus arteries. Especially, the surplus artery that ascended after arising from the caudal region of the aorta and common iliac artery has been reported to interfere with the ascent of a horseshoe kidney. 21) Therefore, we believe the existence of this surplus artery had a role in preventing ascent of the horseshoe kidney of our case also. However, from our analyses we found no significant correlation between the position of the lower end of the horseshoe kidneys and the number of surplus arteries or the number of surplus arteries that arose from the aorta or common iliac artery below the upper end of the isthmus. We conjectured that ascent of the horseshoe kidney was not necessarily prevented by the many surplus arteries; other factors besides the number of surplus arteries influenced the amount of interference with its ascent. Additionally, the left upper pole of our horseshoe kidney was the lowest of all the horseshoe kidneys listed in Table 1A. In our case, we found large splenomegaly. Thus, we suggest that it is necessary to consider additional influences that determine of the position of the kidney. From an embryologic point of view on the morphological characteristics of horseshoe kidney, it has been suggested that its formation occurs until the fifth week of life of an embryo, when its ascent and internal rotation begins. 19,21,23) The existence of surplus arteries in the horseshoe kidney reflects the continuously changing blood supply to the developing kidney during the course of its ascent from the pelvis to its final position. 19) The present study indicated the particular distribution characteristics of the surplus arteries; that is, the surplus arteries which arose from the aorta above the upper end of the isthmus more often entered into the right or left kidney, and the surplus arteries which entered into the isthmus more often arose from the aorta below the upper end of the isthmus. This shows that just after a kidney s ascent begins, the arteries enter into the kidney from its various regions such as its anterior, posterior and inferior surfaces; after the kidney has partially ascended, the arteries that enter into the kidney from each hilum are generated, with the possibility of becoming normal renal arteries. In a horseshoe kidney, the ventrally facing hilum and passage of the ureter on its ventral surface shows its abnormal rotation caused by the fusion of its lower poles. Ueyama et al. 5) discussed that because most previous studies reported that the surplus arteries that arise from the caudal region of the aorta and common iliac artery ran approximately toward the right above, that rotation of the horseshoe kidney does not take place. However, on the other hand, these investigators found in their case that after running to the right behind the isthmus, a surplus artery came around the ventral side and entered into the right kidney, indicating its partial rotation. In our present
7 A case report and analysis of position and arteries in horseshoe kidney 13 case, although surplus arteries A5, A7 and A8, which arose from the caudal region of the aorta or the left common iliac artery, ran approximately toward the right above, because the surplus artery A6 ran similarly to that in the Ueyama report, 5) partial rotation of the right kidney might have occurred. References 1) Bauer SB. Anomalies of the kidney and ureteropelvic junction. In: Walsh PC, Retik AB, Vaughan ED, Wein AJ, editors. Canpbell s urology. 7th ed. Volume 2. Philadelphia: WB Saunders, 1998; ) Murakami G. Urinary system. In: Sato T, Akita K, editors. Anatomic variations in Japanese. Tokyo: University of Tokyo Press, 2000; (in Japanese). 3) Basar H, Basar R, Basar MM, Erbil M. The comparison of the incidence of horseshoe kidney in autopsy cases versus urologic patient population. Okajimas Folia Anat Jpn. 1999; 76: ) Yohannes P, Smith AD. The endourological management of complications associated with horseshoe kidney. J Urol. 2002; 168:5 8. 5) Ueyama T, Ito Takao, Tsuruo Yoshihiro. An autopsy case of horseshoe kidney. J Wakayaka Med Soc. 2008; 59: (in Japanese with English summary). 6) Yakeishi A, Saga T, So H, Tetsuka M, Araki Y, Kobayashi S, Yamaki K. A case of horseshoe kidney with surplus renal arteries. Kurume Med J. 2007; 54: ) Nakamura Y, Yi SQ, Iimura A, Terayama H, Naito M, Itoh M. Morphological observation of the horseshoe kidney with special reference to the vascular system in 2 Japanese cadavers. Okajimas Folia Anat Jpn. 2005; 82: ) Yoshinaga K, Kodama K, Tanii I, Toshimori K. Morphological study of a horseshoe kidney with special reference to the vascular system. Anat Sci Int. 2002; 77: ) Chen H, Hayakawa D, Emura S, Ozawa Y, Yano R, Shoumura S. A case of the horseshoe kidney. Okajimas Folia Anat Jpn. 2001; 78: ) Aida K, Saga T, Yamaki K, Doi Y, Hirata T, Tanaka K, Harada H, Yoshizuka M. A case of horseshoe kidney. Kurume Med J. 1997; 44: ) Shoumura S, Emura S, Utsumi M, Chen H, Hayakawa D, Yamahira T, Tamada A, Terasawa K, Aoki T, Sato K, et al. Two cases of the horseshoe kidney. Acta Anat Nippon. 1992; 67:226 9 (in Japanese). 12) Konishi M, Kikuchi M. A case of persistent left superior vena cava with horseshoekidny. Acta Anat Nippon. 1991; 66: (in Japanese with English summary). 13) Kosugi K, Koda M, Kageyama I, Fukushima O, Takeuchi S, Hayakawa T, Kato S, Yamashita H. Horseshoe kidney A case report. Jikeikai Med J. 1991; 38: ) Nagashima S, Tanaka I, Yamaki K, Hiromatsu S, Hiranuma S, Naruse I, Yashihara M, Miyazaki M. A case of the horseshoe kidney. J Kurume Med Assoc. 1990; 53: (in Japanese with English summary). 15) Sekine G, Ohmori T, Kodama J, Toh H. Horseshoe kidney found in a female cadaver. Okajimas Folia Anat Jpn. 1990; 66: ) Inoue K, Hashimoto. A case of horseshoe kidney. Tsurumi Univ Dent J. 1988; 14: (in Japanese with English summary). 17) Isomura G, Kubo K, Uematsu H. Ramified pelves and their blood supply of the horseshoe kidney in 2 Japanese. Anat Anz. 1988; 167: ) Ohkubo M, Ichikawa S, Odajima G, Uchino S. An autopsy case of horseshoe kidney. Okajimas Folia Anat Jpn. 1981; 57: ) Moore KL, Persaud TVN. The developing human. Clinically oriented embryology. 6th ed. Philadelphia: WB Saunders, 1998; ) Drake RL, Vogl AW, Mitchell AWM. Gray s anatomy for students 2nd ed. Philadelphia: Churchill Livingstone, 2009; ) Takeshige Y, Takaoka C, Yasunari T, Abiru M. A case of horseshoe kidney. J Kurume Med Assoc. 1966; 29:540 9 (in Jpanese). 22) Kitagawa T, Takeuchi K, Kimura S, Muramatsu H, Shimada K. One case of the horseshoe kidney. Acta Anat Nippon. 1979; 54:93 8 (in Japanese with English summary). 23) Boyden EA. Description of a horseshoe kidney associated with left inferior vena cava and disc-shaped suprarenal glands, together with a note on the occurrence of horseshoe kidneys in human embryos. Anat Rec. 1931; 51:
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