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Rom J Morphol Embryol 2014, 55(3 Suppl):1111–1122 ISSN (print) 1220–0522 ISSN (on-line) 2066–8279 ORIGINAL PAPER A morphometric study of multiple renal arteries in Greek population and a systematic review KONSTANTINOS NATSIS 1) , GEORGE PARASKEVAS 1) , ELENI PANAGOULI 2) , ATHANASIOS TSARAKLIS 2) , EVANGELOS LOLIS 2) , MARIA PIAGKOU 2) , DIONYSIOS VENIERATOS 2) 1) Department of Anatomy, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece 2) Department of Anatomy, Medical School, National and Kapodistrian University of Athens, Athens, Greece Abstract The aim of the study was to determine the distribution patterns of multiple renal arteries, evaluate how they are affected by gender and bilateral asymmetry and proceed on a systematic review. Two hundred and six kidneys from 103 Greek cadavers (53 males and 50 females) were investigated. The number and pattern of multiple renal arteries were determined according to side, gender and level of origin. The distances between the main renal and first multiple renal arteries were also measured. Multiple renal arteries were present in 11.2% of the kidneys. No statistically significant difference was found between side and gender (p>0.05). The incidence of multiple renal arteries was 87% unilaterally and 13% bilaterally. As regards the multiple renal arteries, a single artery was detected in 83%, two in 13% and three in 4.3%. In 30.4% (7/23) of the kidneys, there was a short common trunk (<1.5 cm), early dividing into the main renal artery and a thinner artery. Multiple renal arteries on the left side seemed to emerge lower than the right ones and displayed a greater variability at their origin. In the systematic review, we detected the patterns of multiple renal arteries which were classified according to population, gender, side and specimen (cadaveric, radiological or transplant). The awareness of morphology and topography of the multiple renal arteries is important in order to achieve a safe pre and intraoperative management of the renal vascular supply. Keywords: kidney, renal artery, origin, variation, race, gender. Introduction The arterial supply of the kidneys is quite variable. Except the main renal artery (RA), the presence of one or more additional RAs unilaterally or bilaterally is the commonest arterial anatomical variation of the kidneys [1]. Several terms have been used for multiple renal arteries (MRA) [2–5], such as “accessory” [1, 6–15], “supernumerary” [16, 17], “supplementary” [18, 19], “extra” [20–22], “aberrant” [23], “ectopic” [24], “plural” [25] and “additional” [9, 26, 27]. Geyer and Poutasse (1962) [28] mentioned that the term “aberrant” should be used for arteries originating from other vessels than abdominal aorta (AA), even though urologists use this term for the vessels that compress the pelvis or ureter. The incidence of MRA presents a wide variability with a range from 8.7 to 75.7% (median 28.2%) [26]. The MRA are commonly detected unilaterally (30%) than bilaterally (10%) [1, 29] and their incidence presents racial diversity [18, 26]. Although individuals with multiple vessels are normal, the MRA presence may potentially complicate the transplant surgery, RA embolization or angioplasty, the reconstructive management of AA aneurysms and urological interventions [20, 30, 31]. In addition, the higher MRA frequency is related to the risk of renovascular hypertension [32], hydronephrosis [33], ureteropelvic junction obstruction and chronic pyelo- nephritis [23]. Gupta and Tello (2004) [34] mentioned that accessory RAs in 24% of the hypertensive patients represent a vascular anomaly and not a direct cause of hypertension. The objective of this study is to detect the incidence of this abnormality, assess the morphological and topographical layouts in a Greek population, and evaluate how these parameters are affected by gender and bilateral asymmetry. Moreover, a systematic review has been made in order to provide a comprehensive aspect of the topic. Materials and Methods One hundred and three embalmed Greek Caucasian cadavers (53 males and 50 females) aging between 39– 98 years were dissected in the Departments of Anatomy of Aristotle (Thessaloniki) and National and Kapodistrian (Athens) Universities of Greece. The individuals derived from the body donation program after written informed consent and they have no history of previous abdominal injury, pathologic condition or surgery. The Ethics Committees of our Institutions had approved the research protocol. Following the standard method of dissection, the abdominal cavity was opened and organs and retro- peritoneum were removed in order to obtain a better access of the kidneys and their vessels. In some cases, kidneys and related structures were excised en-bloc for a better visualization of the exposed area. Two hundred and six kidneys (106 males and 100 females) were examined and the considered variables were MRA number, gender, side of MRA presence, level of origin of the main RA and MRA and distance between the origins of two arteries. In order to determine the level of origin, the vertebral bodies were divided into upper, middle and lower thirds. All measurements were calculated using a Vernier digital caliper (accuracy, 0.01 mm), and the R J M E Romanian Journal of Morphology & Embryology http://www.rjme.ro/

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Rom J Morphol Embryol 2014, 55(3 Suppl):1111–1122

ISSN (print) 1220–0522 ISSN (on-line) 2066–8279

OORRIIGGIINNAALL PPAAPPEERR

A morphometric study of multiple renal arteries in Greek population and a systematic review

KONSTANTINOS NATSIS1), GEORGE PARASKEVAS1), ELENI PANAGOULI2), ATHANASIOS TSARAKLIS2), EVANGELOS LOLIS2), MARIA PIAGKOU2), DIONYSIOS VENIERATOS2)

1)Department of Anatomy, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece 2)Department of Anatomy, Medical School, National and Kapodistrian University of Athens, Athens, Greece

Abstract The aim of the study was to determine the distribution patterns of multiple renal arteries, evaluate how they are affected by gender and bilateral asymmetry and proceed on a systematic review. Two hundred and six kidneys from 103 Greek cadavers (53 males and 50 females) were investigated. The number and pattern of multiple renal arteries were determined according to side, gender and level of origin. The distances between the main renal and first multiple renal arteries were also measured. Multiple renal arteries were present in 11.2% of the kidneys. No statistically significant difference was found between side and gender (p>0.05). The incidence of multiple renal arteries was 87% unilaterally and 13% bilaterally. As regards the multiple renal arteries, a single artery was detected in 83%, two in 13% and three in 4.3%. In 30.4% (7/23) of the kidneys, there was a short common trunk (<1.5 cm), early dividing into the main renal artery and a thinner artery. Multiple renal arteries on the left side seemed to emerge lower than the right ones and displayed a greater variability at their origin. In the systematic review, we detected the patterns of multiple renal arteries which were classified according to population, gender, side and specimen (cadaveric, radiological or transplant). The awareness of morphology and topography of the multiple renal arteries is important in order to achieve a safe pre and intraoperative management of the renal vascular supply.

Keywords: kidney, renal artery, origin, variation, race, gender.

Introduction

The arterial supply of the kidneys is quite variable. Except the main renal artery (RA), the presence of one or more additional RAs unilaterally or bilaterally is the commonest arterial anatomical variation of the kidneys [1]. Several terms have been used for multiple renal arteries (MRA) [2–5], such as “accessory” [1, 6–15], “supernumerary” [16, 17], “supplementary” [18, 19], “extra” [20–22], “aberrant” [23], “ectopic” [24], “plural” [25] and “additional” [9, 26, 27]. Geyer and Poutasse (1962) [28] mentioned that the term “aberrant” should be used for arteries originating from other vessels than abdominal aorta (AA), even though urologists use this term for the vessels that compress the pelvis or ureter. The incidence of MRA presents a wide variability with a range from 8.7 to 75.7% (median 28.2%) [26]. The MRA are commonly detected unilaterally (30%) than bilaterally (10%) [1, 29] and their incidence presents racial diversity [18, 26]. Although individuals with multiple vessels are normal, the MRA presence may potentially complicate the transplant surgery, RA embolization or angioplasty, the reconstructive management of AA aneurysms and urological interventions [20, 30, 31]. In addition, the higher MRA frequency is related to the risk of renovascular hypertension [32], hydronephrosis [33], ureteropelvic junction obstruction and chronic pyelo-nephritis [23]. Gupta and Tello (2004) [34] mentioned that accessory RAs in 24% of the hypertensive patients represent a vascular anomaly and not a direct cause of hypertension. The objective of this study is to detect the incidence of this abnormality, assess the morphological

and topographical layouts in a Greek population, and evaluate how these parameters are affected by gender and bilateral asymmetry. Moreover, a systematic review has been made in order to provide a comprehensive aspect of the topic.

Materials and Methods

One hundred and three embalmed Greek Caucasian cadavers (53 males and 50 females) aging between 39–98 years were dissected in the Departments of Anatomy of Aristotle (Thessaloniki) and National and Kapodistrian (Athens) Universities of Greece. The individuals derived from the body donation program after written informed consent and they have no history of previous abdominal injury, pathologic condition or surgery.

The Ethics Committees of our Institutions had approved the research protocol.

Following the standard method of dissection, the abdominal cavity was opened and organs and retro-peritoneum were removed in order to obtain a better access of the kidneys and their vessels. In some cases, kidneys and related structures were excised en-bloc for a better visualization of the exposed area. Two hundred and six kidneys (106 males and 100 females) were examined and the considered variables were MRA number, gender, side of MRA presence, level of origin of the main RA and MRA and distance between the origins of two arteries. In order to determine the level of origin, the vertebral bodies were divided into upper, middle and lower thirds. All measurements were calculated using a Vernier digital caliper (accuracy, 0.01 mm), and the

R J M ERomanian Journal of

Morphology & Embryologyhttp://www.rjme.ro/

Konstantinos Natsis et al.

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center of the origin of each artery was taken as recordable point. The incidence of each variable was recorded and descriptive statistics (mean, median, minimum, maximum and standard deviation) were evaluated for the continuous variables. In order to compare the variables, chi-square test and Student’s t-test were applied. For all the analyses, values of p less than 0.05 were accepted as statistically significant and statistical analysis was carried out using IBM SPSS Statistics for Windows version 15.0.

Results

The MRA were detected in 11.2% (23/206) of the kidneys. In 52.2% (12/23), MRA were found on the right and in 47.8% (11/23) on the left side. In males, MRA were detected in 11.3% (12/106), 50% (6/12) on the left and 50% (6/12) on the right side. In females, MRA were present in 11% (11/100), 54.5% (6/11) on the right and 45.5% (5/11) on the left side (Table 1). No statistically significant difference was found between gender and side (p>0.05).

MRA originated from the lateral aspect of AA (Figure 1), except from a unique case where MRA originated from the AA bifurcation. MRA were found bilaterally in 13% (3/23) and unilaterally in 87% (20/23).

A single MRA was detected in 83% (19/23) (Figure 2), two MRA in 13% (3/23) (Figure 3) and three MRA in 4.3% (1/23) (Figure 4). In 30.4% (7/23) of the kidneys, there was a short common trunk (<1.5 cm) early dividing into the main RA and a second thinner artery. One of the kidneys was additionally supplied by a lower polar MRA, arising from AA (Figure 5).

The levels of origin of the main RAs ranged from the upper third of the 11th thoracic vertebral body (T11) to the intervertebral disc of the second and third lumbar vertebrae (L2–L3). The median level was located at the upper third of L2, in 27.2% (28/103) on the left, and at L1–L2 level, in 27.2% (28/103), on the right side (Table 2).

Table 1 – The incidence of multiple renal arteries (MRA) in Greek population according to gender and side

Presence of MRA No. of cases

Percentage No. of cases

Percentage

Gender

R L

Total

M 6 50% 6 50% 12

F 6 54.5% 5 45.5% 11

Total 12 52.2% 11 47.8% 23

M: Male; F: Female; R: Right; L: Left.

Figure 1 – Multiple renal artery (MRA) arising from the abdominal aorta (AA). RRA – Right renal artery, LRA – Left renal artery, LRV – Left renal vein, LK – Left kidney, S – Superior, I – Inferior, M – Medial, L – Lateral.

Figure 2 – One multiple renal artery (MRA) originated from the anterolateral aspect of the abdominal aorta (AA). LRA – Left renal artery, LRV – Left renal vein, LK – Left kidney, S – Superior, I – Inferior, M – Medial, L – Lateral.

A morphometric study of multiple renal arteries in Greek population and a systematic review

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Figure 3 – Posterior aspect of the renovascular pedicle including the two kidneys and their great vessels. RRA – Right renal artery, 1 – First multiple renal artery, 2 – Second multiple renal artery, AA – Abdominal aorta, IVC – Inferior vena cava, RK – Right kidney, LK – Left kidney, S – Superior, I – Inferior, M – Medial, L – Lateral.

Figure 4 – Three multiple renal arteries (MRA) supplying the right kidney (RK). RRA – Right renal artery, 1 – First MRA, 2 – Second MRA, 3 – Third MRA, AA – Abdominal aorta, S – Superior, I – Inferior, M – Medial, L – Lateral.

Figure 5 – Early division of the main right renal artery in the (1) inferior and (2) superior (3) hilar artery with multiple renal artery (MRA) supplying the right kidney (RK). AA – Abdominal aorta, LRA – Left renal artery, S – Superior, I – Inferior, M – Medial, L – Lateral.

Konstantinos Natsis et al.

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The range of MRA origin is summarized in Tables 2 and 3. A greater variability was observed on the left side and left MRA originated lower than the right ones, in the majority of the cases. The distances between the main RA and first MRA ranged from 1.4 to 9.5 cm, on the left side, while on the right side, minimum and maximum distances were 1.1 and 1.6 cm, respectively (mean 3.42±2.66 on the left and 0.51±0.89 cm on the right) (Table 3). A statistically significant difference was found between two sides (p<0.05). On the left side, MRA arose below the main RAs, at a great distance, while on the right side, three MRA originated cranially to the main ones, while all the others originated laterally.

Table 2 – The distribution of the main renal arteries (RA) and multiple renal arteries (MRA) according to the level of origin (in relation to vertebral thirds and intervertebral discs)

Presence

No. of cases of main RA No. of cases of MRALevel of origin

Left Right Left Right

T11u - 1 - -

T11m 1 - - -

T11l - - - -

T11–T12 - - - -

T12u - - - -

T12m 1 - - -

T12l 1 1 - -

T12–L1 - - - 1

L1u 9 15 - 2

L1m 11 18 - 2

L1l 16 23 1 1

L1–L2 20 28 - 2

L2u 28 5 2 2

L2m 9 7 2 1

L2l 4 1 1 1

L2–L3 3 4 1 -

L3u - - 1 -

L3m - - 1 -

L3l - - - -

L3–L4 - - - -

L4u - - - -

L4m - - - -

L4l - - 1 -

L4–L5 - - - -

L5u - - - -

L5m - - 1 -

Total 103 103 11 12

u: Upper; m: Middle; l: Lower vertebral third; T: Thoracic; L: Lumbar.

Table 3 – The distance (in cm) between main renal arteries (RA) and first multiple renal arteries (MRA) and distribution of MRA origin in relation to verte-bral thirds and intervertebral discs (in cases were a caudal and cranial to main renal artery are present, as first MRA was considered the one with most proximity)

Left kidneys Right kidneys

Specimen No. Level of

origin

Distance from

main RA [cm]

Level of origin

Distance from

main RA [cm]

Gender

1. - - L1m 1.1 M

2. L1l 1.8 - - M

Left kidneys Right kidneys Specimen N

Level of origin

Distance from

main RA [cm]

Level of origin

Distance from

main RA [cm]

Gender

3. - - L2m 1.4 F

4. L2m 1.7 L1u 0.5 M

5. - - T12–L1 -0.91 F

6. L3m 2.9 - - F

7. - - L1m 0.7 F

8. L2u 1.4 L2u 1.3 M

10. L4l 7.7 - - F

11. L5m 9.5 - - F

12. L3u 2.3 - - M

13. - - L1–L2 -0.51 F

14. L2u 1.8 L1l 0.7 M

15. L2m 2.2 M

16. L1u -1.11 M

17. L1–L2 0.9 M

18. L2l 3.4 F

19. L2–L3 2.9 F

20. L2u 0.4 F

21. L2l 1.6 F

3.42±2.66 0.51±0.892 1Distances with “-“: above the main renal arteries. 2The distances above the main renal arteries were considered as negative. F: Female; M: Male; u: Upper; m: Middle; l: Lower vertebral third; T: Thoracic; L: Lumbar.

Discussion

RAs (as a pair) supply the kidneys and originate from the lateral wall of AA, at L1 or L2 level, 1.5 cm below the superior mesenteric artery [35]. Usually, the right RA is longer than the left. Each RA runs almost transversely to the renal hilum crossing anterior to the crus of the diaphragm and psoas. The right RA passes behind the inferior vena cava and the right renal vein (RV), whereas the left RA courses behind and above the left RV [36]. During the embryological development, kidneys ascend from the pelvic cavity and take their final position at the lumbar area. Failure of the ascent and persistence of one or more fetal arteries (MRA) may occur [36, 37].

The terminology about the MRA remains obscure and controversial [26, 32]. Graves (1956) [38] argued that no established criterion has been used for the arterial aberrance and the term “multiple” described any additional vessel entering the kidney either originated from AA or the main RA. Merklin and Michels (1958) [18] used the terms “main renal”, “aortic superior and inferior polar” and “renal inferior polar” arteries for the single RA. Geyer and Poutasse (1962) [28] stated that when more than one RAs exist, the additional vessels were called super-numerary, accessory or aberrant and size differences among them exist. Poisel and Spängler (1969) [39] named as “aberrant”, the arteries penetrating the kidney in different areas than hilum, whereas as “accessory or supplementary”, the supernumerary vessels penetrating the hilum. Stephens (1982) [40] claimed that it is incorrect to call these vessels “accessory, aberrant or super-numerary” because they are not extra but essential tissue-sustaining, non-anastomotic arteries, corresponding to the segmental branch of a single RA. Sampaio and Passos

A morphometric study of multiple renal arteries in Greek population and a systematic review

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(1992) [20] used the terms “hilar” for the aortic branch penetrating the hilum, “extrahilar” for the RA branch with an extra-hilar penetration, “superior polar” for the aortic branch penetrating the superior pole and “inferior polar” for the aortic or common iliac artery branch penetrating the inferior pole of the kidney. The authors supported that these arteries should be named “multiple” since the vessels are segmental end-arteries [20, 41]. Satyapal et al. (2001) [26] have named additional, the artery arising from AA and ending in the kidney. Vilhova et al. (2001) [25] used the term “plural” either for “double arteries” similar in diameter, or “triple arteries” different in diameter, originating from AA, entering the kidney through the hilum. In addition, they named “accessory” and “perforated” RAs originating from AA, or the AA major branches (supplying the superior or inferior renal poles) entering through the hilum and outside the hilum, respectively. Bordei et al. (2004) [19] defined “superior and inferior polar”, the arteries distributed to the kidneys’ poles, “main renal”, the larger hilar artery and “hilar supplementary renal”, the smaller one. Holden et al. (2005) [42] named “accessory”, the RA with an aortic ostium separate from the main RA and “supplementary”, the RA with a separate aortic ostium passing directly into the hilum. Daescu et al. (2010) classified the renal arteries as hilar and polar (superior and inferior) arteries. Also, they classified the polar arteries as “solitary” or “pedicular”, the latter one accompanied by a polar vein and a nerve plexus. Moreover, these authors named the polar artery “false supernumerary” if it replaces a segmental artery and “true supernumerary artery” [43].

In our study, the term “multiple” was considered as appropriate for arteries (except the main) that supply the kidney irrespectively of their origin and site of penetration. The term “aberrant” is unclear since it corresponds to: (a) arteries without aortic involvement, (b) arteries entering the kidney through renal cortex except the hilum and (c) the main RA either originating from uncommon sites such as the lower portion of thoracic aorta or coursing abdominally, anteriorly to the inferior vena cava.

Eustachius firstly described the MRA [38]. Since then, several studies have been referred to their incidence and

various limitations appeared, such as: (a) the frequency estimation in respect to individuals or studied kidneys, (b) differences in size of the sample and in methodology (c) MRA definition and (d) the detection of different material. Some authors included in MRA, the polar branches arising from the main RA [18], the branches originating from AA (common iliac arteries, thoracic aorta, major splachnic or parietal AA branches) and cases of early division of the main RA [26]. In many studies, the sample was dissected cadavers or specimens from an autopsy, while in other angiographic studies, the sample was patients. It is argued that the cadaver dissection probably affords a more accurate determination of the number of RA, than aortography [28]. In angiographic studies, the MRA were detected less frequently due to their thickness (diameter <2 mm). Particularly when the MRA originated from AA, they are not detectable and the arteries entering the kidney outside the hilum are frequently confused with the adrenal or capsular arteries [21, 44]. It is noteworthy that the magnetic resonance angiography failed to predict the anatomy of renal arteries in 10% of the patients with MRA compared to angiography, in which the relative incidence was 3% [45].

The first study concerning the MRA incidence revealed an incidence of 30% [18]. Satayapal et al. (2001) [26] estimated the MRA incidence in 28.1%, after reviewing data from 1883 to 1999. In the present study, it was made an effort to collect all relevant studies from 2000 until nowadays and those before 2000, which were not evaluated [26]. The MRA incidence was recorded in different populations (Table 4) and ranges from 4% to 61.5% (mean 23.3%). The frequency was estimated according to specimen – cadaveric (28.2%), radiological (21.8%) and transplant (20.4%). It is obvious that a variable MRA incidence is pointed among the populations and that within the same population exists a wide range of MRA incidence (in Brazilians: 18.5–61.5% and in Turks: 14.5–27%). Such discrepancies could be attributed to the size and the origin of the sample and the methodology for MRA documentation. In our study, in a Greek population, the MRA incidence was estimated in 11.2%.

Table 4 – The incidence of multiple renal arteries (MRA) according to population and specimen

MRA Author(s) Year

Percentage N/Total (Total) Population Specimen

Natsis et al. (Present study) 11.2% 23/206 Greek C

C et al. [46] - (1 CR) C

Talović et al. [47] 46.2% 18/39 Bosnian C (fetal)

Tao et al. [48] 14.5% 55/378 Chinese R

Harraz et al. [49] 14.5% 108/731 Egyptian T

Amirzargar et al. [50] 15.1% 76/502 Iranian T

Aristotle et al. [51] 13.3% 4/30 Indian C

Santos Soares et al. [52] 12% 6/50 Brazilian C

Budhiraja et al. [53] 59.5% 44/74 Indian C

Johnson et al. [54] 36.1% 107/302 Caribbean R

Parimala [55] - (1 CR) C

Malgor et al. [56] 30% 200/672 R

Bertoldi et al. [57]

2013

- (1 CR) R

Aragão et al. [58] 21.7% 13/60 Brazilian C (fetal)

Gümüş et al. [59] 27% 443/1640 Turkish R

Himmel et al. [60]

2012

- (1 CR) R

Konstantinos Natsis et al.

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MRA Author(s) Year

Percentage N/Total (Total) Population Specimen

Hung et al. [61] 17% 17/100 Taiwanese T and R

Krishnasamy et al. [62] - (1 CR) C

Laouad et al. [63] 27.02% 70/259 French T

Mendoza et al. [64] - (3 CR) T

Perla [65] - (2 CR) C

Sezer et al. [66] 14.1% 35/249 Turkish T

Ali Mohammed et al. [67] - (1 CR) C

Sungura [68]

2012

11.3% 23/204 Kenyan R

Chabchoub et al. [69] 21.2% 44/208 Tunisian T

Costa et al. [70] 18.5% 47/254 Brazilian T

Gupta et al. [13] 28.3% 17/60 Indian C

Kapoor et al. [71] 12% 21/171 Canadian T

Mamatha and D’Souza [15] - (2 CR) C

Palmieri et al. [41] 61.5% 123/200 Brazilian R

Rao Rachana [72] - (1 CR) C

Satyanarayana et al. [14] - (1 CR) C

Tyson et al. [73]

2011

23% (510) T

Budhiraja et al. [74] 15% 15/100 Indian C

Gupta et al. [75] - (2 CR) C

Hlaing et al. [76] 4% 2/50 Malaysian C

Koplay et al. [5] - (2 CR) R

Ogeng’o et al. [77]

2010

14.3% 51/356 Kenyan C

Glodny et al. [78] - (2 CR) R

Gurses et al. [79] - (2 CR) C

Kumar et al. [22] - (1 CR) C

Patasi and Boozary [80] - (1 CR) C

Pestemalci et al. [81] - (2 CR) C

Zağyapan et al. [82]

2009

42%* 63/150 Turkish R

Kok et al. [45] 21% 60/288 Dutch T

Nayak [83] - (2 CR) C

Raheem et al. [84] - (1 CR) C

Saldarriaga et al. [27] 25% 97/390 Colombian C

Shoja et al. [17] 43.2% 35/81 Iranian R

Tarzamni et al. [1]

2008

24.8% 58/234 Iranian R

Gesase [16] - (2 CR) C

Olave et al. [85] - (2 CR) C

Papaloucas et al. [86] 27.4% 59/215 Greek R

Singh et al. [32] 18% (333) Operated kidneys

Zeina et al. [87]

2007

- (1 CR) R

Bakirtas et al. [4] 15% 28/187 Turkish T

Rusu [88] - (2 CR) C

Deepthinath et al. [11] - (1 CR) C

Ozkan et al. [21] 14.5% 248/1710 Turkish R

Ozmen et al. [89] - (1 CR) R

Satyapal et al. [26]

2006

- (1 CR) R

Ciçekcibaşi et al. [31] 25% 45/180 Turkish C (fetal)

Holden et al. [42] 26% 52/200 New Zealanders R

Kadotani et al. [90, 91] 14.1% 48/340 Japanese T

Kocabiyik et al. [10] - 1 CR C

Şener et al. [92] - 2 CR R

Weld et al. [93]

2005

37% (73) C

Bordei et al. [19] 20.9% 57/272 Romanian C

Gupta and Tello [34] 14.1% (370) R

Gürkan et al. [94] 14.8% 17/115 Turkish T

Janschek et al. [95] 19.8% 47/238 Austrian C

Khamanarong et al. [3] 18.4% 98/534 Thais C

Talović et al. [96]

2004

25.8% 55/213 Bosnian R

Bayramoglou et al. [9] 2003 - (2 CR) C

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MRA Author(s) Year

Percentage N/Total (Total) Population Specimen

Bude et al. [97] 17% (87) R

Hsu et al. [98] 21.5% (353) T

Oh et al. [99]

2003

9.7% (62) T

37.1% 62/167 African

35.3% 24/68 Whites

18.5% 5/27 “Colored” Satyapal et al. [26]

17.4% 31/178 Indian

C and R

Vilhova et al.* [25] 25.7% (70) R

Vilhova et al.** [25]

2001

31.8% 21/66 Ukrainian R

Wozniak [100] 1999 11.2% 17/152 Polish C

Kuo et al. [101] 1998 33.1% (124) T

Choi et al. [102] 13% 65/500 Korean T

Platt et al. [44] 1997

31.6% (307) R

Bulić et al. [103] - (2 CR) C

Goscicka et al. [7] 1996

12.1% 34/280 Polish C (fetal)

Atasever et al. [6] - (1 CR) C

Sampaio and Passos [20] 1992

30.4% 81/266 Brazilian C

Berland et al. [104] 22% (50) R

Desberg et al. [105] 1990

24% (55) R

Awojobi et al. [2] 1983 - (1 CR) R

Giavroglou [106] 1982 17.6% 327/1855 Greek R

Armstrong et al. [107] - (1 CR) R

Tisnado et al. [108] 1979

- (1 CR) R

Odman and Ranniger [109] 1968 8.3% (24) R

Nathan [110] - (7) C

Merklin and Michels [18] 1958

19.5% 36/185

Marshall [111] 1951 56% (800) C

Ronstrom [112] 1947 18% 36/200 Afro-American C

27.8% 40/144 White American C Lloyd [113] 1935

20.4% 33/162 Afro-American C

Adachi [114] 1928 22.8% 77/338 Japanese C

Iijima [115] 1925 25% 15/60 Japanese C

Gerard [116] 1911 22% 63/287 French C

Levi [117] 25.5% 49/1921 Italian C

Seldowitsch [118] 1909

17.7% 53/300 Russian C

Kater [119] 1901 - (2 CR) - C

Brewer [120] 1898 28.1% 85/302 White American C

C: Cadavers; R: Radiological; T: Transplants; CR: Case report. *In respect to individuals and not the kidneys. Otherwise, the incidence is 24.33%. In parenthesis appears the total number of the sample used.

Two previous studies in Greeks reported a higher incidence of 17.6% [106] and 27.4% [86], presumably due to the larger size of the sample and the geographical differences among the populations as well as because the findings were angiographic and not cadaveric as occurred in our study. Therefore, the MRA incidence is influenced not only by race but also by hereditary and environmental factors (geographical background, ethnicity and social differences) [121].

In our study, although the MRA presence on females was in preponderance compared to that of males, the difference was not statistically significant according to

gender. Several authors observed a higher incidence in males than females [26, 27, 32, 96, 114], whereas others concluded in opposite results [7, 25, 58]. A statistically significant preponderance was revealed in males [22, 28] (Table 5). Furthermore, there is a great controversy about the MRA incidence according to side. Some investigators reported that MRA are frequently left-sided [8, 10, 16, 19, 21–24, 27, 41, 70, 82, 114, 122, 123], while others contradict that the right side predominates [1, 3, 7, 13, 15, 21, 32, 42, 45, 59, 78, 79] (Table 5). In addition, MRA were found to occur bilaterally with a variable incidence from 1.6 to 41% [1, 21, 25, 41, 65, 90, 91, 124].

Table 5 – The number of multiple renal arteries (MRA) according to gender (Males – M and Females – F) and side (Right – R and Left – L)

No. of MRA (%)

Gender Side Author(s) Year MRA (%)

M (%) F (%) R (%) L (%)

Adachi [114] 1928 1 MRA: 68/338 (20.1%)

2 MRA: 9/338 (2.7%) Total: 77/338 (22.8%)

65/274 (24%) 12/64 (19%)

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No. of MRA (%)

Gender Side Author(s) Year MRA (%)

M (%) F (%) R (%) L (%)

Ronstrom [112] 1947 1 MRA: 36/200 (18%) (16%) (20%)

Geyer and Poutasse [28] 1962 1 MRA: 100/744 (13.4%)

2 MRA: 11/744 (1.5%) Total: 111/744 (14.9%)

(12.9%) (17%)

Goscicka et al. [7] 1996

1 MRA: 30/280 (10.7%) 2 MRA: 3/280 (1.07%) 3 MRA: 1/280 (0.4%) Total: 34/280 (12.1%)

(9.3%) (12.8%) (11.5%) (p<0.05)

(7.7%) (p<0.05)

Satyapal et al. [26] 2001 1 MRA: 102/440 (23.2%)

2 MRA: 20/440 (4.5%) Total: 122/440 (27.7%)

85/257 (33.1%) (p=0.00)

37/183 (20.2%) (p=0.00)

(23.3%) (p=0.04)

(32%) (p=0.04)

Vilhova et al. [25] 2001 1 hilar a.: 4/66 (18.7%)

2 hilar a.: 1/66 (3%) Total: 21/66 (31.8%)

11/36 (30.6%) 10/30 (33.3%) (28.1%) (35.3%)

Khamanarong et al. [3] 2004 1 MRA: 93/534 (17.4%)

2 MRA: 5/534 (0.9%) Total: 98/534 (18.4%)

(20.6%) (14.6%)

Janschek et al. [95] 2004 1 MRA: 39/238 (16.4%)

2 MRA: 8/238 (3.4%) Total: 47/238 (19.8%)

(20.2%) (19%)

Bordei et al. [19] 2004 1 MRA: 54/272 (19.8%) 2 MRA: 3/272 (1.10%)

Total: 57/272 (21%) (40%)* (60%)

Talović et al. [96] 2004 Total: (25.9%) M>F (49.1%) (36.4%)

Holden et al. [42] 2005 1 MRA: 48/200 (24%)

2 MRA: 4/200 (2%) Total: 52/200 (26%)

(36%) (16%)

Ciçekcibaşi et al. [31] 2005 1 MRA: 45/180 (25%) (28.8%) (13.3%) (32.1%) (17.6%)

Ozkan et al. [21] 2006

1 MRA: 231/1710 (13.5%)2 MRA: 15/1710 (0.9%) 3 MRA: 2/1710 (0.1%)

Total: 248/1710 (14.5%)

(p>0.05) (16%)

(p=0.131) (12.9%)

(p=0.131)

Singh et al. [32] 2007 Total: 60/333 (18%) (74.1%)

(p=0.054)

(62.1%) (p=0.269)

Saldarriaga et al. [27] 2008 1 MRA: 87/390 (22.3%) 2 MRA: 10/390 (2.6%) Total: 97/390 (24.9%)

89/338 (26.3%) (p=0.317)

8/52 (15.4%) (22.2%)

(p=0.187) (27.3%)

(p=0.187)

Tarzamni et al. [1] 2008 1 MRA: 53/234 (22.7%) 2 MRA: 5/234 (2.14%) Total: 58/234 (24.8%)

- (32.5%) (p=0.01)

(17.1%) (p=0.01)

Zağyapan et al. [82] 2009 1 MRA: 69/300 (23%) 2 MRA: 4/300 (1.3%)

Total: 73/300 (24.3%)** - (24%) (24.7%)

Budhiraja et al. [74] 2010 1 MRA: 15/100 (15%) - (5.2%)*** (3.1%)

Hlaing et al. [76] 2010 1 MRA: 1/50 (2%) 2 MRA: 1/50 (2%) Total: 2/50 (4%)

- (4%) (4%)

Costa et al. [70] 2011

1 MRA: 42/254 (16.5%) 2 MRA: 4/254 (1.6%) 3 MRA: 1/254 (0.4%) Total: 47/254 (18.5%)

- (8.6%) (9.8%)

Palmieri et al. [41] 2011

1 MRA: 77/200 (38.5%) 2 MRA: 38/200 (19%) 3 MRA: 7/200 (3.5%) 5 MRA: 1/200 (0.5%)

Total: 123/200 (61.5%)

(65%) (p=0.31)

(58%) (p=0.31)

(56%) (p=0.11)

(67%) (p=0.11)

Gupta et al. [13] 2011 Total: 17/60 (28.3%) - (36.7%) (20%)

Aragão et al. [58] 2012 1 MRA: 11/60 (18.3%)

2 MRA: 2/60 (3.3%) Total: 13/60 (21.7%)

(6.25%) (7.2%) (11.7%) (10%)

*The incidence referred only to one MRA; **The authors estimated the incidence according to individuals (42%) and not the kidneys; ***The incidence referred only to double hilar arteries.

In our study, all MRA originated from different levels of AA, except a unique case, which originated from the aortic bifurcation. Many other sites of origin such as lumbar arteries, middle sacral artery [122], (main hilar) renal artery, common or internal iliac, inferior phrenic, gonadal, suprarenal, right colic, 12th intercostal, right hepatic, celiac, superior or inferior mesenteric arteries, or

the lower portion of AA have been reported [3, 107, 122, 125, 126]. Furthermore, the MRA number usually varies from 1–3 (Table 5), however, four [114, 122], five [41] and seven MRA [127] have been documented. In our study, three MRA were detected in 4.3%.

Early division of the main RAs should be considered by the surgeons in patients with MRA, in order to safely

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ligate the main RA in the living donor or perform anastomosis without stricture in receipt area. In such cases, the main RA should be at least 1 cm in length [20]. Such division named “precocious bifurcation” [20] characterized the main RA bifurcation or branching after a course of 1 cm, 1.5 cm [43, 128], or 2 cm [27]. Kadir (1991) [121] stated that the rate of early division in the general population was 15%. The relative incidence was found in 3.5% [90, 91], 6.5–9.6% [129], 8% [21], 10% [128], 12% [42], or 16% [44] in several studies. Sampaio and Passos (1992) [20] “limited” the early division in 1 cm and reported an incidence of 2.6%, whereas Saldarriaga et al. (2008) [27] “expanded” the distance in 2 cm and found an incidence of 13%, (9.4% on the right and 16.5% on the left side). Tarzamni et al. (2008) [1] noted a higher incidence of early branching in 35.9%. In our study, seven (3.4%) cases of early division (<1.5 cm from the aortic origin) were detected.

The two main RAs normally arise from AA, the right originating higher. In 25% of the subjects, a significant disparity in the origin may occur [23]. Kadir (1991) [121] mentioned that in 75%, the RA arises from AA, at L1–L2 level. Beregi et al. (1999) [30] mentioned that in 90%, the RA arose between the L1 lower third and the L2 lower border. Ozkan et al. (2006) [21] reported that in 97–98%, the main RA originated between the upper margin of L1 and lower border of L2. The same notice has been made by Palmieri et al. (2011) [41] in 94.8% on the right and 91.4% on the left side. Zağyapan et al. (2009) [82] found that in 93%, the RA originated from AA (T12–L2 level). Aragão et al. (2012) [58] found that RAs were situated between the lower third of T12 and upper third of L1. As regards the height of aortic origin, Keen (1981) [129] found that the right RA in 48.1% was more than 2 mm above the left, in 19.2% the left was higher and in 32.7% the difference was less than 2 mm. The right RA origin was found cranially, at the same level and caudally to the left RA in 53.3%, 10% and 36.6% [21], 37%, 50% and 13% [30], 72%, 16% and 12% [130], 53.8%, 34.6% and 11.5% [15], 49.2%, 34.4% and 16.4% [27] and 47.36%, 36.84% and 15.8% [58], respectively.

In our study, the median level of the main left RA origin (upper third of L2) according to the vertebral thirds and intervertebral discs was found lower than the right one (L1–L2). In 94.2%, the main RA originated between the upper margin of L1 and lower margin of L2, on each side. Other investigators found the MRA arising between T11 and L4 [18] and L1–L3 vertebrae [96]. Bordei et al. (2004) [19] determined the distance between the aortic origin of the main RA and MRA as highly variable (average 1–2 mm to 4–6 cm). Saldarriaga et al. (2008) [27] noticed an average distance of 7.5±10.5 mm between the first MRA and its origin from the main RA (mean 8.5 mm on the right and 6.5 mm on the left) with these differences being not statistically significant according to side.

As conclusion, MRA are located bilaterally caudal to the main RAs, with the right MRA situated lower than the ipsilateral main RAs compared to the left side. According to Macalister (1883) [122], the first MRA springs from AA near the inferior mesenteric artery and the second one, if existed, near the main one. In our study,

the origins of left MRA present a higher variability than the right ones, while the left MRA emerge from lower levels. Moreover, the left MRA originated below at a greater distance from the main RAs and the right MRA arose in close proximity to the main RAs (mean 0.51± 0.89 cm). These results are in contrast with the findings of Saldarriaga et al. (2008) [27], which reported that the left MRA arose more close to the main RA.

From the embryonic point of view, MRA are consi-dered as persistent entities of the initial nephrotome region. In a fetus of 18 mm, the developing mesonephros, metanephros, suprarenal glands and gonads are vascula-rized by 18–20 segmental branches from AA [18]. The mesonephros extended from the eighth cervical to the 12th thoracic vertebra, is supplied by the “rete arteriosum urogenitale”. The middle group (3rd–5th arteries) gives rise to RAs. The persistence of more than one arteries of the middle group results in MRA [18, 37]. As the embryo grows, there is a relative ascent of the kidneys from the pelvic cavity to the lumbar region. This process is accompanied by changes in the blood supply. Particularly, when the metanephros lies within the pelvic cavity, it receives blood supply from iliac arteries, and when it finally lies at the lumbar region, arterial branches from the iliac arteries to AA supply it [131]. As the kidneys gradually ascent, RAs arise at higher levels of the AA until they finally develop at L2 level. Whereas in humans the MRA represent persistent mesonephric arteries, their presence is the rule in lower animals [122]. Chemical, genetic factors, nutrients and oxygenation are among the factors leading to the regression of the caudal arteries and the persistence of the cranial arteries of the “rete arteriosum urogenitale” [12]. It has been considered that anomalies associated with kidneys rotation are often related to MRA [6] and may be associated with a variety of abnormalities, such as renal lobulation, aberrant gonadal artery and abnormal renal veins [12, 19, 88].

The awareness of existence of one or more MRA is very important, as they might complicate the renal transplantation, and play a significant role in renovascular hypertension, reconstructive surgery of AA aneurysms and uroradiological procedures [12]. It is important the main and MRA to be anastomosed during transplantions, as it is well known that between renal arteries intrarenal cross-segmental anastomoses do not exist [26]. Although kidney grafts with MRA seems to appear disadvantages due to vascular [115] and urologic complications [131], the MRA presence in donor’s kidney does not adversely affect the long-term allograft and the patient overall survival [79, 106]. Hemorrhagic complications, RA thrombosis, and warm ischemia time are significantly higher in patients with MRA [106, 131]. Furthermore, an association between MRA and renovascular hypertension has been reported, but it has not been widely accepted [33, 34]. It seems that there is a correlation between the stenosis of MRA and hypertension [33]. Thus, radiologists and clinicians dealing with the kidney arterial pathology should keep in mind the possible presence of MRA, during balloon angioplasty and stent implantation [30]. The MRA and lower polar arteries commonly coursing anteriorly to the ureteropelvic junction are considered as an etiologic factor of hydronephrosis. However, it is more

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possible that the retroureteral course of MRA leads to hydronephrosis [8]. Radiologists and surgeons should investigate the existence of possible variations in RAs usual pattern preoperatively, as they may lead to important complications [3, 6].

Conclusions

ΜRA is a common but a significant anatomical variant of the renal vascular system, due to their clinical importance. In our sample, the MRA presence was detected in 11.2% and displayed a greater variation on the left than the right side. Because this abnormality plays an important role in kidney transplantations, in radiological, vascular and urological interventions, a detailed presen-tation of MRA incidence was conducted, gathering from the literature a large number of relevant studies in order to create a classification according to population, gender, side and specimen.

Acknowledgments Konstantinos Natsis had full access to all of the data

in the study and takes responsibility for the integrity of data and the accuracy of data analysis.

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Corresponding author George Paraskevas, Assistant Professor, MD, PhD, Department of Anatomy, Medical School, Aristotle University of Thessaloniki, Post Box: 300, 54124 Thessaloniki, Greece; Phone +30 2310 999330, e-mail: [email protected] Received: August 21, 2013 Accepted: November 14, 2014