|Year : 2021 | Volume
| Issue : 6 | Page : 380-392
Benign renal tumors in pediatric age group: Retrospective analysis
Prema Menon1, Katragadda Lakshmi Narasimha Rao1, Saalim Nazki1, Saswati Behera1, Kirti Gupta2, Ram Samujh1, Shailesh Solanki1, Akshay Saxena3, Deepak Bansal4, Amita Trehan4
1 Department of Pediatric Surgery, Postgraduate Institute of Medical Education and Research, Chandigarh, India
2 Department of Histopathology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
3 Department of Radiodiagnosis, Postgraduate Institute of Medical Education and Research, Chandigarh, India
4 Department of Pediatric Hemato Oncology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
|Date of Submission||16-Jun-2020|
|Date of Decision||26-Jul-2020|
|Date of Acceptance||22-Sep-2020|
|Date of Web Publication||12-Nov-2021|
Dr. Prema Menon
Department of Pediatric Surgery, Advanced Pediatrics Centre, Postgraduate Institute of Medical Education and Research, Chandigarh - 160 012
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Background: Benign renal tumors are extremely rare and were studied here. This series also includes a renal teratoma in a horseshoe kidney, probably only the second in the pediatric literature.
Materials and Methods: Retrospective review of children with benign renal tumors operated between 2006 and 2018 at one center.
Results: Twelve patients (M:F ratio 10:2), age range 3 weeks (31-week gestation) to 13 years presented with large palpable renal swelling (n = 12) and hematuria (n = 3). Computed tomography (CT) scan showed features typical of the tumor. Final histopathology (age group [mean]) showed: multilocular cystic nephroma (MLCN) - n = 5 (41.7%), (11–16 months [13.6]); congenital mesoblastic nephroma (CMN) - n = 4 (33.3%) (classic 1, cellular 3) (0.75–5 months [2.125]); mature cystic teratoma - n = 1 (8.3%): (48 months, in a horseshoe kidney), and angiomyolipoma (AML) - n = 2 (16.7%) (144 months [sporadic] and 156 months [tuberous sclerosis]) One patient with cystic teratoma with no calcification on CT scan received pre-operative chemotherapy as fine-needle aspiration cytology (FNAC) reported malignant small blue cell tumor. Nephroureterectomy with Gerota's fascia could be done easily in all without intraoperative complications. Delay in presentation in MLCN and CMN led to increased symptoms and CT scan changes. All patients did well in 1.5–12 years (median 3 years) follow-up including cellular mesoblastic nephroma.
Conclusions: Benign renal tumors often occur in specific age groups but may overlap that of Wilms tumor. Proper interpretation of clinical presentation, CT scan, and FNAC findings help in avoiding preoperative chemotherapy. Upfront nephroureterectomy is curative. Histopathological findings decide further treatment. Children with AML and tuberous sclerosis need lifelong follow-up.
Keywords: Angiomyolipoma, congenital mesoblastic nephroma, kidney, multilocular cystic nephroma, nephroureterectomy, teratoma
|How to cite this article:|
Menon P, Narasimha Rao KL, Nazki S, Behera S, Gupta K, Samujh R, Solanki S, Saxena A, Bansal D, Trehan A. Benign renal tumors in pediatric age group: Retrospective analysis. J Indian Assoc Pediatr Surg 2021;26:380-92
|How to cite this URL:|
Menon P, Narasimha Rao KL, Nazki S, Behera S, Gupta K, Samujh R, Solanki S, Saxena A, Bansal D, Trehan A. Benign renal tumors in pediatric age group: Retrospective analysis. J Indian Assoc Pediatr Surg [serial online] 2021 [cited 2023 Dec 4];26:380-92. Available from: https://www.jiaps.com/text.asp?2021/26/6/380/330364
| Introduction|| |
Renal tumors constitute 7% of all childhood tumors. More than 90% are Wilms' tumor (WT) with an incidence of 8.2 cases per 1 million children <15 years of age. Non-Wilms malignant renal tumors include clear cell sarcoma of the kidney (CCSK), rhabdoid tumors, and renal cell carcinoma. Benign tumors of the kidney, due to their rarity, are likely to be misdiagnosed as WT and may receive unnecessary preoperative chemotherapy. In this series, the benign renal tumors managed by the authors over a period of 13 years were analyzed, including the challenges faced during diagnosis and outcome after surgery.
| Materials and Methods|| |
This was a retrospective review of all the cases of benign renal tumors in children from the neonatal period up to 15 years of age that were surgically managed in a single unit of a tertiary care pediatric surgery center from 2006 to 2018. The cases were operated by two senior pediatric surgeons with several years of surgical experience. Approval was obtained from the Institute Ethics Committee (NK/5948/Study/080) to publish retrospectively collected data and waiver for the consent of patients to participate in the study. The patient identifiers in images have been obscured.
Cases were initially evaluated on the basis of history and clinical examination. Baseline blood investigations such as hemogram, urea and creatinine were performed in all cases. Radiological diagnosis was initially by ultrasonography of kidney, ureter, bladder (USG KUB) region followed by contrast enhanced computed tomography (CECT) scan of the abdomen in all patients. Fine-needle aspiration cytology (FNAC) was performed where there was suspicion of WT based on clinical features or interpretation of CECT abdomen. CECT chest was performed only in those cases where imaging and FNAC suggested WT.
Patients underwent radical nephroureterectomy with Gerota's fascia with the removal of the entire ureter until just above the vesicoureteric junction. Wherever there was pre-operative suspicion of WT or nodes were prominent, lymph node sampling was done during surgery and areas documented. Intra-operative findings, which were noted were ease of removal of kidney, infiltration or adherence to local structures, rupture, uncontrolled bleed, vascular injury, hypotension requiring inotropic support, pneumothorax, etc. The immediate postoperative course of the patients was noted from admission files. The excised specimen was sent for histopathological examination (HPE), which was taken as the final confirmation of the benign nature of the disease and inclusion in the study group. Therefore, patients who received pre-operative chemotherapy based on clinical interpretation, CECT, and FNAC but were found to have benign renal tumor on HPE were also included. All malignant renal tumors were excluded. All histopathology slides were reviewed. Follow-up information was collated from data maintained in the outpatients.
| Results|| |
A total of 12 patients were identified in the 13-year study period. There was a male predominance (M:F ratio; 10:2). The mean age was 35.38 ± 8.48 months (0.75–156 months). Based on nephrectomy HPE, the benign renal tumors encountered were multilocular cystic nephroma (MLCN) in 5 (41.7%); congenital mesoblastic nephroma (CMN) in 4 (33.3%); teratoma (mature cystic) in 1 (8.3%) and angiomyolipoma (AML) in 2 (16.7%). The images of each patient are placed in the same order as in [Table 1] with figures of children with MLCN, CMN, Teratoma and AML given as [Figure 1], [Figure 2], [Figure 3], [Figure 4], respectively. The intra-operative pictures of one child with MLCN (S.No. 4) could not be traced.
|Figure 1: Images of Multilocular cystic nephroma patients: Computed tomography scans (a, c, e, f, h, i, j and k), gross specimen and cut sections (b, d, g, l and m) and histopathology slides (n). (I) Low magnification depicting multiple variably sized cysts (H and E, x100); (II) Fibrous septa dividing cysts and lacking immature nephrogenic elements, (H and E, x200); (III) High magnification showing low cuboidal cells forming the cystic lining (H and E x400)|
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|Figure 2: Images of Congenital Mesoblastic nephroma patients: Computed tomography scans (a, b, d, g, j; white arrow in a, d, g shows typical hypodense crescent shape in periphery), intra-operative photographs (e and k), specimen/cut sections (c, f, i and l), Histopathology (m). (I) Low magnification depicting fascicles and whorls of bland spindled myofibroblasts and thin collagen fibers entrapping the normal tubules (H and E, x200); (II) Fascicles composed of plump, atypical spindle cells with abundant cytoplasm and vesicular nuclei (H and E, x200); (III) Cellular mesoblastic nephroma depicting areas with brisk mitotic activity (arrow, H and E, x400); (IV) MT stain reveals fine collagen within the stroma (MT x400). MT: Masson's trichrome|
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|Figure 3: Images of Mature teratoma patient: Computed tomography scans (a and b), intra-operative photographs (c and d), specimen (e), Histopathology (f). (I) Elements from 3 germ layers (H and E, x100); (II) Irregularly shaped glands lined by goblet cells in loose mesenchyme (H and E, x100); (III) Glands lined by goblet cells (H and E, x200); (IV) Interface of tumor with kidney|
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|Figure 4: Images of Angiomyolipoma patients: abdominal swelling crossing midline (a), Computed tomography scans (b and f), Magnetic Resonance Imaging brain (c), tuberous sclerosis skin lesions (d), specimen/cut section (e and g), Histopathology (h). (I) Low magnification showing triphasic elements composed of myoid spindle cells, mature adipose tissue and dysmorphic thick walled blood vessels; (II) High magnification depicting vascular component is in the form of thick walled hyalinized blood vessels without elastic lamina (H and E x400); (III) Fascicular pattern formed by sheets of spindle cells (H and E x400); (IV) Immunoreactivity for HMB45 noted within the neoplastic cells (immunoperoxidase x100)|
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All patients had normal blood urea and serum creatinine. All had a palpable, non-tender mass in the renal fossa, which crossed the midline in one case each of MLCN, CMN, and AML. [[Table 1]; S.No. 5, 9, 11]. Three (25%) patients gave a history of hematuria: MLCN (S.No. 1), and both the children with AML (S.No. 11, 12). In children with CMN, the tumor was antenatally detected in one case (25%). There was premature birth in 2 other cases (50%), with the youngest a 31-week pretermer who got operated 3 weeks after birth [[Table 1]; S.N. 6–9].
Two cases of MLCN, (S.No. 2 and 3) were referred to us as cystic WT based on imaging. FNAC showed benign columnar cells. There was herniation into the pelvis of the kidney in 2 of the 5 patients with MLCN [[Table 1] (S.No. 1 and 5) and [Figure 1]a, [Figure 1]b, [Figure 1]k, [Figure 1]l and [Figure 1]m], one of whom presented with an episode of hematuria. Two other patients (S.No. 8, 9) who underwent FNAC to rule out WT were correctly interpreted as CMN.
In case no. 10, FNAC was reported as malignant small round blue cell tumor, consistent with WT. CECT abdomen impression was cystic fat-containing WT or cystic teratoma in a horseshoe kidney. Serum alpha-fetoprotein was 1.8 ng/ml. The CECT chest showed two small (<3 mm) subpleural nodules in the left lower lobe lung and on review by radiologist were considered too small to be considered metastases. He received four cycles of vincristine and actinomycin-D based on FNAC before surgery with no reduction in the size of swelling on USG. He underwent right nephroureterectomy with right Hemi isthmusectomy. No plane of differentiation was noted with the upper pole of the kidney or pelvicalyceal system [Figure 3d].
Case 11 (AML) had clinical features suggestive of tuberous sclerosis complex (TSC) like mental retardation, generalized hypopigmented spots and adenoma sebaceum [Figure 4a and d]. Magnetic resonance imaging brain [Figure 4c] had shown tubers. Referral CECT scan and FNAC were reported as WT. FNAC repeated at our center because of the rapidly enlarging abdominal mass was reported as clusters of malignant cells with moderate pleomorphism and interpreted as renal cell carcinoma. He underwent an uneventful nephroureterectomy of a large renal mass occupying nearly the entire abdomen. Nephroureterectomy with Gerota's fascia was possible in all cases without tumor rupture/spillage or injury to adjacent structures. There was no hemodynamic instability in any of the cases during surgery.
In 2 cases of CMN (S.No. 7, 8) focal capsular breach with extension into perinephric fat was noted on HPE. Lymph node sampling done at the time of nephroureterectomy in S.No. 3 and 8–11 were found to be reactive with no tumor infiltration.
S.No. 11 presented 1 month after nephroureterectomy with adhesive intestinal obstruction, which was managed conservatively. Multiple small AMLs were noted in his right kidney at 3-year follow-up, but renal function tests were normal. Both the children with AML have been handed over to adult urology and nephrology services for long-term followup. All other patients had no complaints in the immediate or long term follow-up of 1.5–12 years (median 3 years) with no evidence of recurrence at the local or distant site, including patients with teratoma and cellular CMN.
| Discussion|| |
WT is the most common renal tumor in the age group of 6–119 months (median 36 months). Other renal tumors, both benign and malignant, are rare. In centers following SIOP protocol with initial chemotherapy followed by nephrectomy, a child with a benign tumor may unnecessarily receive chemotherapy unless they are <6 months age. Occasionally, a benign tumor may require only partial nephrectomy. Therefore, it is imperative to know the diagnostic features of benign renal tumors of childhood.
CMN is the most common renal neoplasm diagnosed in the neonatal age with a high prevalence before 2 months of age. Nearly 75% manifest by 6 months age.,,, Diagnostic confusion with WT and CCSK is likely when they present after 2 months of age. In our study, 3 of the 4 cases presented by 2 months of age with only one case being operated at 5 months age, all of whom presented with a palpable flank mass. We observed that the imaging, external appearance and cut section of the tumor was different in the child who presented at 5 months age compared to all the others who were operated by 2 months age. [Figure 2] In this child, the tumor had a mutilobulated appearance, covered by a thin transparent capsule and crossed the midline. The delay in seeking surgical treatment may have led to progressive increase in size and necrosis within the tumor. On gross appearance, CMN and CCSK may look similar. However, CCSK has a similar age distribution as WT. In a 2.5-months-old male baby, who underwent nephroureterectomy, the solid, homogenous tumor with the whorled appearance and firm consistency on cut section and the age of the child prompted a diagnosis of CMN. The HPE however showed typical features of CCSK showing monotonous array of oval to spindle cells with vacuolated cytoplasm and indistinct borders set against a variably myxomatous stroma and the baby was excluded from the study. The histopathologic classification of CMN includes three subtypes: classic (24%), cellular (66%), and mixed (10%)., Barrantes et al reported a M:F ratio of 5:4 in conventional CMN and 2:1 in the atypical cellular CMN. In our study also, the M:F ratio in cellular CMN was 2:1. An overview of 306 published cases showed that CMN has an extremely good prognosis. It has a relapse rate of 4%, mostly seen in cellular CMN. Howell et al. in 1982 reported relapse in one of 51 cases, 6 months after surgery, which was associated with intraoperative rupture. After surgical excision and chemotherapy, their patient was free of the disease at 18-month follow-up. In our study, 3 of the 4 cases (75%) had a cellular subtype on HPE with one (S.No. 6) showing local adherence and a highly vascular capsule. Significantly enlarged draining vessels were noted in 2 cases of cellular CMN (S.No. 6, 9). Focal capsular breach with the involvement of perinephric fat was seen in both cellular (S.No. 7) and classic subtype (S.No. 8) on HPE. In Furtwaengler et al.'s study, patients with cellular CMN were significantly older with a median age of 112 days compared to classic CMN with a median age of 6 days. However, in our series, both ends of the age spectrum had cellular CMN. Babies >3 months of age with intra-operative tumor rupture and extensive extrarenal infiltration, incomplete resection, prior open biopsy, positive lymph node, i.e., stage III disease, cellular subtypes or aneuploidy may have to be cautiously considered for additional chemotherapy.,,, We were able to perform radical nephrectomy in all our cases with no intraoperative spill or capsular tear which is the only line of management required for the majority of patients. CMN is known to have a short risk period for relapse. Our patients were closely followed up with clinical examination and ultrasound in the first 1 year after surgery with no evidence of recurrence during this period and late follow-up.,,,,
MLCN is a benign mixed mesenchymal and epithelial neoplasm of the kidney, which lacks solid areas., The present study had five cases of MLCN, all males, aged 11–16 months at the time of surgery. In a systematic literature review, Granja et al. noted a median age of 18 months and a male predominance of 60.8% in those aged <10 years. In our study, the weight was below normal for age in 3 children, probably due to the pressure effect of the swelling on the gastrointestinal tract. There was a complaint of hematuria in one case (20%) and abdominal pain (20%) in another where the tumor had involved the renal pelvis. [Figure 1a, b, k, l and m]. In a review of 155 cases, including all age groups, patients presented with abdominal mass in 54 (35.2%), abdominal pain in 29 (18.7%), and hematuria in 11 (7.1%). In our series, the tumor was located in the upper and midpole in 3 cases and the lower and mid pole in 1 case. Almost the entire kidney was involved in only one case (S.No. 5), who was symptomatic for 11 months with the mass crossing the midline. His initial USG at a peripheral center had suggested multicystic dysplastic kidney (MCDK) with no function on diuretic renography. He presented to us with failure to thrive, gross abdominal distension, and abdominal pain. The progressive increase in size in MLCN differentiates it from MCDK, where the swelling should reduce with time. Complete nephroureterectomy was performed in all our cases, as mid pole involvement was universal. Both SIOP and NWTS protocols give similar advice with no other treatment required.
The Bosniak classification system of radiology based on morphological changes in renal cysts, presence of calcification, content, and contrast enhancement may help in evaluating complex cystic renal masses. However, it is difficult to differentiate MLCN from malignant cystic partially differentiated nephroblastoma (CPDN), cystic Wilms and a subset of cystic renal cell carcinoma.,, The presence of some solid component on imaging indicates WT. Histopathology of excised nephrectomy specimen is the final answer. In CPDN, features are intermediate between that of the benign MLCN and the malignant cystic WT. The inability to take a core biopsy in cystic masses adds to the therapeutic dilemma. In MLCN, the cysts contain clear fluid with chemical composition similar to serum and have normal cytology. In three cases where FNAC was performed at our center, the benign nature of the disease was confirmed.
Renal AMLs are uncommon. Rapid growth of the mass in childhood and adolescence is noted in TSC., Mesenchymal cells are thought to be the precursor cell for all the components of AML. Development of tortuous vessels and aneurysms which are prone to rupture can lead to hematuria, retroperitoneal hemorrhage, and encroachment into normal renal parenchyma, leading to chronic renal disease. Warncke et al. analyzed 145 patients of TSC and noted an AML incidence of 50.3%. Annual renal USG screening is recommended after 11 years of age for prophylactic treatment and avoiding presentation with hemorrhage or shock. In our series, S.No. 11 with TSC presented at 13-years age with pain abdomen, an episode of hematuria and a large renal swelling crossing the midline. The child had been referred with a preoperative CECT and FNAC reported as WT. The CECT scans had shown no areas of fat attenuation. A repeat FNAC at our center suggested renal cell carcinoma, and he underwent total nephrectomy on the left side.
Partial instead of total nephrectomy is preferred in AML, especially in those with TSC. The criteria for intervention in AML are symptomatic lesions, size >4 cm, associated aneurysm >5 mm and suspicion of malignancy. Selective arterial embolization using different agents have been described in acute hemorrhage, refractory hemodynamic instability as well as prophylactically to shrink the tumor, but have a recurrence rate of 11–40%., Both the patients in this study underwent total nephrectomy in view of large tumor size, symptoms, location of tumor, and in one case, a pre-operative suspicion of malignancy.
Intrarenal teratoma of the kidney is exceedingly rare with only around 30 cases reported in the literature, with the majority being benign. Idrissi-Serhrouchini et al. reported a 6-month-old girl with immature teratoma in a pelvic kidney. They also reviewed 15 other cases of renal teratoma, 9 of them in the pediatric age group. Mochizuki et al. reported the first case of an immature teratoma arising in the right lower pole and isthmus of a horseshoe kidney. This was similar in tumor location to our patient (S.No. 10), who appears to be only the second case of intrarenal teratoma reported in a horseshoe kidney in the pediatric age group. Apart from horseshoe kidney, association with double ureter, prune belly syndrome, and renal dysplasia have been described. For pure immature teratomas, complete excision of the tumor mass alone is sufficient with 3-year event-free survival rate of >85%. Mature teratomas though benign have a propensity for malignant transformation, thus making long-term follow-up paramount. Our patient is doing well at a follow-up period of 18 months.
Biopsy in many centers is recommended for renal tumors in children >10 years age and where there is clinical and radiological suspicion of non-WT. Due to the presence of a dedicated well-established department of cytopathology and the use of SIOP protocol in our center, FNAC is routinely performed for all cases of WT and others where pre-operative tissue diagnosis is required. Although the accuracy may not be equivalent to core needle biopsy, the advantages are that it is an easy and quick procedure not requiring anesthesia in a small child. To reach more representative areas, image-guided biopsy is preferred. To overcome the handicap of fragmented material, it is centrifuged, thus increasing the cellular yield and processed to form a paraffin cell block. This and the addition of immunocytochemistry improves diagnostic accuracy. Where there is a doubt, core needle biopsy is performed. In this series, while FNAC accurately diagnosed CMN and MLCN, it was not so with teratoma and one case of AML. Renal cell carcinoma is known to occur in TSC patients but with an incidence of <2%. Studies have shown similarity on hematoxylin-eosin staining between epithelioid variant of AML and renal cell carcinoma. WT has heterologous components of blastemal, stromal and epithelial origin, similar to renal teratoma due to a common origin from mesodermal metanephrogenic blastema. WT is also known to be more common in horseshoe kidneys.
In CMN, a hypodense crescent-shaped width was typically found to surround the lesion in 3 of our 4 cases, all of whom had presented in <2 months age [Figure 2a, d and g]. This is not often reported in the literature. Chen et al. have highlighted this typical double-layer sign and attribute it to slow blood flow and delay in filling of the contrast in the peripheral blood sinuses. We also observed that unlike CMN, which tends to grow centrifugally and involve the entire kidney, MLCN tends to involve one or other pole of the kidney compressing the normal kidney in a cranial or caudal direction. Progressive increase in the size of the swelling leading to tumor crossing the midline can occur in benign tumors also which may be due to internal bleeding (S.No. 11) or delay in treatment (S.No. 5, 9). Dilated pelvicalyceal system in the remaining kidney may occur due to the local pressure effect (S.No. 10) or the mass herniating into the renal pelvis (S.No. 5). Small subpleural or pulmonary nodules <5–6 mm in size may be due to previous respiratory tract infections, and a careful history should be elicited to avoid mistaking them for metastases.
The SIOP protocol recommends MLCN and CPDN be treated primarily by surgery, and cystic WT by a combination of neoadjuvant chemotherapy and surgery. However, some authors feel that surgery should be the first line of treatment even when the initial diagnosis is cystic WT due to pre-operative radiological fallacies. We agree with this approach as we had similar issues while dealing with teratoma with a predominant cystic component. Rarely, if the lesion is <4 cm in size and confined to one pole, partial nephrectomy or tumorectomy may be considered as in some cases of metanephric adenoma or inflammatory pseudotumor.
There should be no misconception that benign renal tumors are small. All the tumors seen in this series and most seen in the literature are large and palpable at presentation.,,,,, An overview of these tumors with typical characteristics are summarized in [Table 2]. The excellent long-term outcome can be expected in nearly all benign renal tumors provided complete excision is safely achieved.
| Conclusions|| |
There is a lot of similarity in the presentation of benign renal tumors and WT with incidental diagnosis or presentation with a progressively increasing large, flank mass being common. Occasionally weight loss, hematuria, and pain may be present. The general condition is usually well preserved unless there is delay in presentation. Tumors presenting outside the age spectrum of WT may be easier to diagnose, whereas those presenting around the same time as a WT create confusion. The treating surgeon should be aware of the clinical features and the unique identifying features on CECT. These tumors tend to be well defined, mobile, single, unilateral, mass lesions with no features of invasion, lymphadenopathy, renal vein or inferior vena cava thrombus and metastases. There is invariably some normal ipsilateral renal parenchyma. In doubtful cases, needle biopsy in expert hands is useful to reach a correct preoperative diagnosis.
The authors acknowledge the help of Dr K.S. Sodhi, & Dr. A. Bhatia (Department of Radiodiagnosis and Imaging); and Dr. R. Srinivasan (Department of Cytology) in patient management.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2]