The nutcracker phenomenon (NCP) also known as left renal vein (LRV) entrapment, focuses on the compression of the LRV most commonly between the abdominal aorta (AA) and superior mesenteric artery (SMA). It is a rare variation encountered in the renal vasculature anatomy. The resulting clinical manifestation of this phenomenon is termed the nutcracker syndrome (NCS). The common signs and symptoms may present as proteinuria, blood in urine, pelvic, and abdominal pain which may worsen during menstruation in women, pain in the lower left abdomen, fatigue, headaches, pain, and swelling of the scrotal veins in men. It gets its name as it is the same as the compression of a nut by a nutcracker. Hematuria occurs due to renal venous hypertension which eventually leads to the rupture of the walls of veins into the collecting system.[1,2,3]
Certain types of nutcracker phenomena have been described by various authors. There are three known types of NCP: (1) anterior NCP in which LRV gets compressed in between AA and another abdominal artery, (2) posterior NCP (or pseudo-NCS) where LRV is compressed by AA and vertebral bodies, (3) mixed type which includes a wide range of blood vessel changes. More rare conditions are posterior and right-sided NCSs.[2,3]
J. C. Grant was the first one to provide an anatomic description of NCS in 1937, whereas the first case presentation was reported by El Sadr and Mina in 1950. De Schepper used the term nutcracker for the first time in his article in 1972 followed by Chait who described the nutcracker pattern relating to two arms of the nutcracker compressing the LRV in between AA and SMA. There are other theories of causes that can lead to NCS including pancreatic neoplasms, retroperitoneal tumors, para-aortic lymphadenopathy, and overarching testicular artery, while the right-sided NCS has been stipulated due to compression of a gravid uterus.[2,3,4]
NCP is a rare finding as reported by various authors. The aim of this study is to know the prevalence of NCP in the population of Uttarakhand. In some patients, if NCP presents clinical symptoms of hematuria, proteinuria, renal injury, and thrombosis, clinicians rarely link it to the possibility of NCS since it is quite underdiagnosed. Therefore, to prevent any serious complications and misdiagnosis, we need to describe such rare syndromes and understand their prevalence of the same. This would only further help the clinical practitioners to improve care coordination, management, differential diagnosis, appropriate evaluation, and to improve the outcomes for patients affected by NCS.
MATERIALS AND METHODS
This is a cross-sectional (retrospective study) done in the population of Uttarakhand, India. The study was conducted from April 2021 to May 2022 in the Department of Anatomy, Government Doon Medical College, Dehradun after obtaining Institutional Ethics Committee approval (GDMC/IEC/2022/REVISED/15 dated 31/05/2022). The sample size was calculated by the following formula:
N: population size, p: proportion = 0.5
e: margin of error, z: z score = 1.96
This study was conducted during the routine dissection of five cadavers for undergraduate teaching and 160-CT angiography images procured from the department of radiology.
A total of 14 renal veins which included four accessory renal veins (aRVs) (one left and three right) were analyzed from cadaveric dissection and 98 renal veins which included 10 aRVs (three left and seven right) were analyzed from CT angiography films.
The kidneys were dissected and removed according to Cunningham's manual practice of anatomy.
Renal veins were explored along with its tributaries. After displacing the veins, arteries were exposed and studied along its branches. The arrangement of hilar structures was evaluated.[5,6]
Computed tomography angiography
One hundred and sixty-slice computed tomography (CT) angiography was also used to understand the renal vein tributaries and variations in their pattern. CT angiography images were retrospectively analyzed to study the renal vasculature. The CT images were reconstructed using the Vitrea software, to study the 3D volume rendering (VR) images. The images were interpreted by the radiologist.
For every patient undergoing CT angiography, the scanning parameters were as follows:
The data were tabulated and prevalence was calculated using Microsoft Excel 2019.
CT angiography images for renal vasculature during the year April 2021 to May 2022 were included in the study.
CT films/cadavers showing any pathology which disturbed the course of the renal vein were excluded from the study.
During the routine dissection classes of undergraduate MBBS students, five cadavers (three males and two females) were dissected. None of the cadavers showed any pathology disturbing the course of the renal vein; therefore, all five cadavers were included in this study. Two cadavers had only one renal vein on the right and left side each. One cadaver had one aRV on both sides. Two cadavers had one aRV only on the right side. Therefore, a total of 10 main renal veins (five left and five right) and four aRVs (one left and three right) were analyzed. Out of 14 renal veins, NCP was shown in two renal veins. As shown in Figure 1, the left-sided mixed NCP was seen in one cadaver (female) in which the LRV was seen compressed by the anterior inferior segmental branch of the left renal artery (LRA) anteriorly and posteriorly by the main trunk of the LRA. The right renal vein (RRV) of this cadaver was normal in its course. In Figure 2, right-sided mixed NCP was seen in a cadaver (male) in which two RRVs were seen among which an accessory RRV was seen compressed by the anterior division in front and the posterior division posteriorly of the right renal artery (RRA). On the left side, there was only one renal vein which was normal in its course in this cadaver.
After applying the exclusion and inclusion criteria, only 44 CT films were included for analysis in this study (36 males and eight females). A total of 49 (five cadavers and 44 CT angiography) cases were analyzed, of which 36 cases had single renal veins on both sides. Two cases showed one aRV each on the left side. Four cases were seen to have one aRV each on the right side. One case had one aRV on both sides. Only one case was seen to have two aRVs on the right side. A total of three cases in CT angiography showed NCP. As shown in Figures 3 and 4, left-sided NCP was seen in two cases in which the left-sided renal vein was compressed by the anterior inferior segmental branch of LRA anteriorly and posteriorly by the main trunk of LRA. The course of RRV was normal in both cases. As shown in Figure 5, right-sided NCP was seen in one case in which RRV was compressed anteriorly by the anterior division and posteriorly by the posterior division of RRA. The LRV showed a normal course in this case. All cases in our study were of mixed NCP as shown in Table 1.
The NCS and NCP have been alternatively used by authors in various literature. However, NCS includes the clinical presentation due to NCP, therefore, the term NCS should be considered only for patients who show symptoms due to NCP. De Schepper is given the credit for the term “nutcracker Syndrome”. NCP is quite rare and the incidence rate seems to vary among different age groups. The exact prevalence is also not defined due to insufficient epidemiological data. Some authors believed it to be more common in females although later studies showed no correlation with gender.[4,7,8]
The anterior or the classical NCS has a higher incidence than the posterior retroaortic NCS. Some authors have reported the increase in height of the body alongside vertebral maturation as one of the causes of the manifestation of NCP. It occurs due to a decrease in the angle between the SMA and the AA, thus resulting in the compression and entrapment of the renal vein.[9,10,11]
J. C. Grant was the first anatomist to describe a clinicopathological case of the entrapment of LRV along with the duodenum between the SMA and AA in a 60-year-old female patient named Lilian K in 1937. It is stated that the renal veins develop from the aortic collar, subcardinal veins, supracardinal veins, and the anastomosis of the cardinal veins. The anterior anastomosis gives rise to the LRV meanwhile the posterior anastomosis gets degenerated. Any abnormality with the degeneration leads to the abnormal presence of retroaortic or circumaortic renal vein. Sawant et al. discovered a rare case of hilar (mixed) NCP in which the LRV was getting compressed by the anterior inferior segmental branch of the LRA due to its serpentine course. Three of our findings match with their hilar NCP. Bao-Zhong et al. explained the case of a 20-year-old male with NCS, who presented with the symptoms of renal hypertension and hematuria due to the compression of left-sided inferior vena cava (IVC).[7,12,13]
Wasniewska et al. presented an unusual case with double IVC along with right-sided NCP in a 42-year-old female patient who came with symptoms of pain abdomen. Polguj et al. analyzed a case of a 58-year-old female patient with compression of LRV between SMA and RRA. It was an incidental finding the patient showed no symptoms of NCS, instead had been admitted for cholelithiasis.[14,15,16]
Ribeiro et al. did a study on a total of 295 patients to study the prevalence of LRV entrapment signs on CT angiography. The mean calculated aortomesenteric angle was 58.7 in men and 53.1 in women. The beak sign and angle were 15.3% and 9.8%, with a greater prevalence in women. The study showed no difference between sexes, although they analyzed a positive correlation with younger age.
Other risk factors and causes of renal vein entrapment include pancreatic neoplasms, retroperitoneal lymphadenopathy, and tumors. Various considerations also include aortic dissection simultaneously with duodenal obstruction due to SMA syndrome. NCS does not show a clear natural history as its prognosis may vary. It can lead to thrombosis and renal injury, gross hematuria, leading to anemia, and proteinuria if left untreated or in young children, it might resolve spontaneously.[3,7]
Renal veins show a lot of variations and its knowledge is important for surgeons, radiologists, and urologists, to deal with renal trauma, renal artery embolization, vascular reconstruction, and during renal transplantation. The clinicians can further prevent any accidental injury and recognize such variations.
In recent years, there has been a significant rise in the diagnosis of this phenomenon in patients with symptoms of hematuria or proteinuria. NCP does not always manifest in its related symptoms, it may come as an incidental finding or only diagnosed when the patient may present with NCS. With recent development in diagnostic modalities, CT abdomen is the investigation of choice for most abdominal symptoms. NCP may result in dilatation of the renal hilum and congestion in the left kidney and may manifest as NCS with symptoms such as hematuria, proteinuria, anemia, varicocele, and abdominal pain. NCP is a rare case and often an incidental finding, therefore, most authors report this phenomenon as a case. Not much exploration has been initiated solely on the NCP. Therefore, there is a discrepancy in the prevalence of cases found in the present study in comparison to that of other authors. In the present study, we have used the modality of 160 slice CT scanner to study the angiography images of renal vasculature by 3D construction of anatomical images in volume-rendered images to accurately identify any abnormalities to reach the highest sensitivity and specificity.
Since the NCP is a rare occurrence not a lot of research has been done in this topic, hence, leading to unknown exact prevalence and incidence of the same. Therefore, there is a lack of data to compare the study with significantly.
Although the NCP and NCS are a rare occurrence, it has been determined that it was possibly underdiagnosed due to a lack of the proper advanced imaging and diagnostic modalities. In the present study, we discovered NCP during routine dissection and by CT angiography films. The prevalence of NCP was calculated to be around 10.2% and all were variants of mixed NCP.
Therefore, it is important to highlight such rare variations as these are of clinical importance, especially in the field of surgery.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
The authors thank Dr. Avantika Ramola (Senior Resident, Department of Radiodiagnosis) for sharing her clinical knowledge with the cases of NCP. We also thank Dr. Harish Basera (Assistant Professor, Department of Internal Medicine, Government Doon Medical College) for sharing his clinical experiences with cases of renal vascular diseases.
The authors also sincerely thank those who donated their fetuses to science so that anatomical research could be performed. Results from such research can potentially increase humankind's overall knowledge which can then improve patient care. Therefore, these donors and their families deserve our highest gratitude.
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