Post-transplant pelvic arteriovenous malformation in a living kidney transplant recipient

Abstract

Arteriovenous malformations are rare vascular anomalies that may be congenital or occur secondary to trauma or surgery. Here, we report a rare case of a pelvic arteriovenous malformation that gradually enlarged after living-donor kidney transplantation. The recipient, a man with end-stage kidney disease from IgA nephropathy, underwent ABO-compatible living kidney transplantation from his father at 6 years prior. A non-contrast computed tomography scan at 3 years post-kidney transplant incidentally revealed a pelvic vascular lesion that progressively enlarged upon serial imaging. Subsequent contrast-enhanced computed tomography suggested a saccular pelvic arteriovenous malformation, prompting further evaluation with selective angiography. Angiography revealed multiple arterial feeders flowing into the right internal iliac vein via abnormal vascular channels. These changes were likely due to ligation and transection of the right internal iliac vein during kidney transplantation, resulting in sac-like dilation and arteriovenous malformation. Endovascular treatment was performed by venously accessing the dilated right internal iliac vein via the left external and internal iliac collaterals, and embolization was successfully achieved using coils and ethanol. Although arteriovenous malformations can result from surgery, this case represents the first reported instance of a pelvic arteriovenous malformation after kidney transplantation. This report highlights a rare and important vascular complication of kidney transplantation.

Introduction

Arteriovenous malformations (AVMs) are abnormal vascular structures formed by direct connections between the arteries and veins that bypass the capillary system. Although AVMs can occur throughout the body, including the head and neck, trunk, limbs, and internal organs, pelvic AVMs are extremely rare [1]. They may be congenital or acquired, and occur typically after trauma or surgery [2]. Pelvic AVMs can cause non-specific symptoms such as pelvic pain, tenderness in adjacent organs, dysuria, urinary frequency, hematuria, and in some patients, high-output cardiac failure. Early diagnosis is challenging, and clinical vigilance is essential [3, 4].

In kidney transplantation (KT), the allograft is typically implanted in the right iliac fossa with vascular anastomoses to the external or internal iliac artery (IIA) and external iliac vein. Common surgical complications include vascular thrombosis, ureteral obstruction, ureteral leakage, and surgical site infection [5]. Although pelvic AVMs have been incidentally identified during pre-transplant evaluations [6], de novo cases have not been reported after KT.

Herein, we present a rare case of a living donor KT recipient diagnosed with a pelvic AVM at 6 years postoperatively. The AVM was successfully treated with endovascular embolization and was likely associated with prior vascular manipulation during KT surgery.

Case description

A man in his 40 s was admitted for endovascular treatment of a pelvic AVM. Six years prior, he underwent ABO-compatible living donor KT from his father for end-stage kidney disease secondary to IgA nephropathy. Post-KT, he received immunosuppressive therapy with methylprednisolone, mycophenolate mofetil, and tacrolimus (target trough 3–5 ng/mL). Additional medications included nifedipine, cilnidipine, bisoprolol, doxazosin, indapamide, olmesartan, febuxostat, atorvastatin, rabeprazole, and alfacalcidol for hypertension, dyslipidemia, and hyperuricemia, respectively. The allograft function was stable, with a serum creatinine of 1.4–1.7 mg/dL. Pre-KT pelvic computed tomography (CT) revealed no vascular dilatation or abnormal collateral venous pathways (Fig. 1A). Non-contrast CT performed 3 years prior had revealed a vascular-like mass (21 × 54 mm) in the right pelvis (Fig. 1B).

Fig. 1.

Pelvic AVM images. A Contrast-enhanced CT before KT yields no abnormal findings in the pelvic vessels (white circles). B Non-contrast CT performed 3 years previously reveals a cystic mass shadow in the right pelvis, similar to vascular dilatation (white arrow). C A contrast-enhanced CT image in the arterial phase indicating the right IIV with surrounding microvascular proliferation (white arrow). D Slab MIP image reconstructed from a contrast-enhanced CT scan to facilitate viewing of the abnormal vascular run (white arrow). E The 3D reconstructed pelvic AVM based on contrast-enhanced CT (white arrow indicates the sac and collateral vessels). F The fourth lumbar artery flows into the nidus (black arrow) through the microvessels (white arrow). G The inferior mesenteric artery flows into the nidus (black arrow) through the microvessels (white arrow). H The left IIA flows into the nidus (black arrow) through the microvessels (white arrow). I The median sacral artery flows into the nidus (black arrow) through the microvessels (white arrow). J The right inferior epigastric artery flows into the nidus (black arrow) through the microvessels (white arrow). K The right IIV flows into the left IIV (black arrow) through collateral vessels (red arrow). L Schematic representation of the transplanted vascular anastomosis and AVM. The two renal arteries are end-to-end anastomosed with the two branches of the IIA, and the renal vein is anastomosed with the right IIV that has been ligated and transected (pink, part of the allograft; red arteries; blue veins; red meshes, microvessels; black wavy lines, vascular anastomosis and transection). 3D, three-dimensional; 4th LA, fourth lumbar artery; AVM, arteriovenous malformation; CT, computed tomography; IEA, inferior epigastric artery; IIA, internal iliac artery; IIV, internal iliac vein; IMA, inferior mesenteric artery; KT, kidney transplantation; MSA, median sacral artery; slab MIP, slab maximum intensity projection

Given the concerns regarding radiation and contrast-induced nephrotoxicity, follow-up was conducted using interval non-contrast CT. As the lesion enlarged to 27 × 64 mm, contrast-enhanced CT revealed a cystic pelvic mass with multiple arteries flowing into the dilated right internal iliac vein (IIV), which formed a nidus suggestive of a pelvic AVM (Fig. 1C–E). Six months prior, selective angiography identified feeders from the fourth lumbar (Fig. 1F), inferior mesenteric (Fig. 1G), left internal iliac (Fig. 1H), median sacral (Fig. 1I), and right inferior epigastric arteries (Fig. 1J) to the right IIV. During KT, the right IIV was ligated and transected to mobilize the external iliac vein, resulting in rerouted venous drainage through the pelvic collaterals to the left IIV (red arrow in Fig. 1K). Pre-KT imaging indicated no AVM, and the patient was diagnosed with a postsurgical pelvic AVM (type IIa, arterial-dominant nidus) [7]. The schematic is presented in Fig. 1L.

Although the patient was asymptomatic, embolization was performed because the AVM showed progressive enlargement, raising concerns about rupture, high-output heart failure, and potential future challenges with minimally invasive transcatheter therapy. Given its proximity to the ipsilateral allograft, the procedure was also intended to prevent steal phenomena and preserve graft function. Under general anesthesia, a guidewire and microcatheter were inserted via pelvic collaterals into the sac (Fig. 2A). The nidus was embolized using 10 detachable coils (Fig. 2B). After coil embolization, residual flow remained in the AVM cavity, and thus, two injections of 100% ethanol (1 mL each) were administered. The flow was completely occluded, and the outflow tract pressure decreased from 28/23 to 6/3 mmHg (Fig. 2C). Related laboratory data are presented in Table 1. Post-embolization, the patient experienced mild pelvic pain, although no adverse events were reported, and he was discharged without complications.

Fig. 2.

Pelvic AVM treatment images. A The catheter is passed from the left internal iliac vein through the collateral vessels to the interior of the sac (black arrow). B The AVM is embolized with coils implanted into the nidus. C Contrast medium has been injected; however, there are no findings of the contrast medium being washed out of the sac with arterial blood flow, only pooling around the embolus is apparent (black arrow). AVM, arteriovenous malformations

Table 1.

Clinical data from pre- to post-treatment

	Outpatient stable baseline	At contrast-enhanced CT scanning	Pre-angiography	Pre-treatment	Immediate post-treatment	1 month post-treatment	2 months post-treatment	8 months post-treatment
Hemoglobin (g/dL)	12.9	11.8	11.9	10.7	11.2	11.7	12.4	11.7
D-dimer (μg/mL)			0.4	0.5	3.2	1.0	0.8	0.4
Creatinine (mg/dL)	1.6	1.4	1.68	1.75	1.66	1.91	1.59	1.77
Estimated glomerular filtration rate (ml/min/1.73m2)	38.2	43.9	36.0	34.4	36.5	31.3	38.2	33.8
Blood urea nitrogen (mg/dL)	21.5	23.0	35.9	46.3	24.0	33.9	29.7	39.3
C-reactive protein (mg/dL)	3.21	0.32	0.05	0.33			0.13	0.16
N-terminal pro-brain natriuretic peptide (pg/mL)	204	254					200	98.2
Urine-protein	±	−	−		+	−	−	−
Urine-occult blood	−	±	−		+	−	−	−
Urine protein/creatinine ratio (g/gCr)	0.088	0.122	0.076		0.381	0.063	0.075	0.058
Urine albumin/creatinine ratio (g/gCr)	0.012	0.018					0.005	0.004

CT, computed tomography

Discussion

Herein, we reported a case of a newly developed pelvic AVM following KT. AVMs typically occur in the extremities, head, or neck. Pelvic AVMs account for less than 2% of cases, making them exceedingly rare [1]. Previous reports of pelvic AVMs in KT recipients describe cases identified during pre-transplant evaluations [6]. In that report, a pelvic AVM was detected on contrast-enhanced CT prior to transplantation, whereas in our case, the AVM was incidentally discovered six years after transplantation. Additionally, the previously reported patient had a history of pulmonary embolism, while our patient presented with an asymptomatic pelvic AVM. Furthermore, in the previous report, conservative management was chosen for the pelvic AVM. Therefore, to the best of our knowledge, this is the first reported case of a postoperative pelvic AVM arising at the site of vascular ligation that was successfully treated with transcatheter embolization.

AVMs can be triggered by several surgical procedures [8, 9]. Although the mechanism of AVM formation after vascular dissection, anastomosis, or surgical procedures remains unclear, possible triggers include anastomosis of the graft renal artery to the right IIA and IIA ligation that may redirect the arterial supply from the left IIA or other arteries, inducing abnormal collateral vessels and AVM formation around the right IIV. It is also possible that a small communication between the right and left IIVs, undetectable on contrast-enhanced CT, existed prior to transplantation. In that case, the right IIV may have remained patent without thrombosis after ligation, thereby promoting abnormal flow and subsequent formation of an AVM.

The fundamental treatment strategy for type IIa AVMs, as observed in the present case, involves occlusion of the draining veins using coils or core-removed guidewires [7]. Because the AVM was located deep within the pelvis and surgical resection would have been highly invasive, a transcatheter embolization procedure was selected as the treatment approach. As residual blood flow was detected around the coils, an additional injection of 100% ethanol was administered. Transcatheter embolization is a minimally invasive and effective treatment for AVMs, including those with complications such as large size or high-flow states [10, 11]. However, treatment failure can occur in some cases, requiring surgery [12]. In our patient, although asymptomatic, the AVM enlarged over time. Early intervention provides clinical benefits by preventing the need for invasive procedures. Shorter pathways such as AVMs may impair renal hemodynamics and lead to decreased kidney function, although recovery has been reported following AVM treatment [13]. In this case, serum creatinine levels showed only minimal change, and no significant improvement in allograft function was observed. This may be because the AVM originated from vessels not directly supplying the allograft, resulting in a lesser hemodynamic impact on the graft than initially expected. Notably, levels of N-terminal pro-brain natriuretic peptide, a marker of heart failure, gradually decreased after embolization, suggesting that closure of the progressively enlarging AVM was associated with favorable changes in cardiac hemodynamics. Although the present case was successfully treated, long-term follow-up is required to monitor the impact on allograft function and the potential recurrence of the AVM.

In conclusion, we reported a rare case of new-onset pelvic AVM in a KT recipient who was successfully treated with coil embolization and ethanol without complications. Although extremely rare, clinicians should recognize the potential for pelvic AVMs to develop after KT.

Author contributions

M.O. contributed to case conceptualization, clinical management, data collection, figure preparation, and manuscript drafting and revision. F.K. contributed to manuscript revision and figure preparation. M.Y. contributed to case conceptualization and manuscript advice and revision. Y.S. contributed to developing pathophysiological hypotheses, critical input, and manuscript revision. R.N., K.S. and H.S. contributed anatomical input on vascular structures and hypothesis development. S.W. contributed to clinical examination and treatment, manuscript revision, and figure preparation. S.H. and H. M. contributed to clinical examination, treatment, and manuscript revision. All authors participated in the final approval of the manuscript.

Funding

No funding was obtained for this case report.

Data availability

All clinical data are available from electronic medical records at St. Marianna University Hospital. The data supporting the findings of this study are available from the corresponding author upon request.

Declarations

Conflict of interest

Ryuto Nakazawa has received lecture fees from Chugai Pharmaceutical Co., Ltd. and Astellas Pharma Inc. for giving talks on prostate cancer, unrelated to this case report. The other authors have no conflicts of interest to declare.

Ethical approval

All procedures involving human participants were performed in accordance with the ethical standards of the institutional and/or national research committee at which the studies were conducted and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. The reported clinical and research activities are consistent with the Principles of the Declaration of Istanbul, as outlined in the Declaration of Istanbul on Organ Trafficking and Transplant Tourism.

Patient consent

No information identifying individual patients was published, and personal information was protected. The patient provided informed consent for the publication of this case report.