Received: 12 January 2017
Accepted: 22 June 2017
DOI: 10.1111/vsu.12728
ORIGINAL ARTICLE
Phrenicoabdominal venotomy for tumor thrombectomy in dogs with adrenal neoplasia and suspected vena caval invasion
Philipp D. Mayhew BVM&S, DACVS Ingrid M. Balsa DVM | | William T. N. Culp VMD, DACVS | Allison L. Zwingenberger DVM, MAS, DACVR, DECVDI ®
Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, California
Correspondence
Philipp D. Mayhew, Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, One Shields Road, Davis, CA 95616. Email: philmayhew@gmail.com
Abstract
Objective: To describe a technique for tumor thrombectomy by phrenicoabdominal venotomy in dogs with adrenal neoplasia and suspected caval invasion and to report complications and outcomes associated with the procedure.
Study design: Retrospective case series.
Animals: Eight client-owned dogs with invasive adrenal tumors.
Methods: Medical records of dogs diagnosed with adrenal tumors with extension of thrombus into the phrenicoabdominal vein (PAV) and vena cava were reviewed. Cases where phrenicoabdominal venotomy without cavotomy for thrombus resection was performed were included. Data collected from the medical records included sig- nalment, clinical signs, physical examination findings, diagnostic imaging results, preoperative laboratory testing, surgical technique, surgical and postoperative compli- cations and outcome.
Results: Phrenicoabdominal venotomy was successful in removal of vena caval thrombosis in 7 of 8 dogs. In one case, an attempt was made to remove a large vena caval thrombus through a distended PAV resulting in fragmentation of the thrombus and the need to extend the incision into the vena cava. In all dogs, complete removal of tumor thrombus was achieved. Two dogs died in the perioperative period, one from cardiopulmonary arrest and a second from bronchopneumonia and pancreatitis. The remaining 6 dogs were discharged from the hospital.
Conclusion: Thrombectomy through a phrenicoabdominal venotomy may obviate the need for a cavotomy in a subset of dogs with invasive adrenal neoplasia.
1 INTRODUCTION |
Adrenalectomy has traditionally been viewed as one of the more challenging procedures in canine surgical oncology. In dogs, most adrenal masses are either adrenocortical in origin or pheochromocytomas derived from the chromaffin cells of the adrenal medulla.1 Invasion into the surrounding vascula- ture is not uncommon and is usually initiated by phrenicoab- dominal vein (PAV) penetration with propagation of tumor thrombus into the vena cava. In the more severe cases, the tumor thrombus will ascend toward the hepatic vena cava and eventually progress into the right atrium. Propensity for
vascular invasion is dependent on tumor type with pheochro- mocytomas being more likely to be associated with tumor thrombus formation than adrenocortical tumors. Published data suggest that pheochromocytomas demonstrate vascular invasion in 33%-55%2-5 of cases whereas adrenocortical tumors invade the vasculature in 2%-22% of cases.3-6
Invasion into the PAV alone can usually be managed by simple en bloc resection of the adrenal mass and PAV with the latter being sealed or ligated at its point of entry into the vena cava. Vena caval invasion has traditionally been man- aged by cavotomy, thrombus removal, and primary sutured closure of the vena cava.1,4 This approach requires temporary
inflow occlusion usually accomplished with placement of Rummel tourniquets followed by partial cross clamping of the vena cava during caval wall repair. The approach can be technically challenging and can be associated with signifi- cant hemorrhage and morbidity.3-6
In a small subsection of cases, diagnostic imaging reveals the presence of PAV thrombi that have extended into the vena cava but which have remained modestly sized. In these cases, removal of the thrombus in its entirety is still highly desirable to avoid distant embolism if the tumor thrombus is dislodged. However, if cavotomy can be avoided in these cases it is possible that blood loss may be minimized and that prolonged inflow occlusion to the involved caval seg- ment may be avoided.
This study describes a technique for removal of tumor thrombi from the vena cava by phrenicoabdominal venotomy alone. The aims of the study were to describe the technique and report the outcomes of surgery in a cohort of dogs that underwent the procedure.
2 MATERIALS AND METHODS |
2.1 Case selection |
Medical records of dogs that underwent adrenalectomy between April 2010 and December 2016 were examined. Dogs in which the presence of vena caval tumor thrombus was diagnosed or suspected based on abdominal ultrasound or contrast-enhanced computed tomography (CECT) scans and that underwent phrenicoabdominal venotomy to attempt tumor thrombus removal in association with adrenalectomy were included in the study.
2.2 | Diagnostic evaluation
Medical records were searched and the following data were collected: signalment, clinical history, physical examination findings, results of diagnostic imaging, and laboratory testing (complete blood count, biochemistry screen, and urinalysis). Endocrinologic evaluation included in most cases ≥1 labora- tory tests including a urine cortisol:creatinine ratio, adreno- corticotropic hormone (ACTH) stimulation test, endogenous ACTH assay, low-dose dexamethasone suppression test and/ or high-dose dexamethasone suppression test, urine normeta- nephrine:creatinine ratio and urine metanephrine:creatinine ratio.
The results of diagnostic imaging were reported. Tho- racic radiographs were taken using a Eklin EDR6 digital radiography system (Sound, Carlsbad, California), abdomi- nal ultrasound examinations were performed using a Philips HDI unit (Philips, Bothell, Washington) using either a 5-8 MHz microconvex or a 12-15 MHz linear transducer.
Computed tomography (CT) studies were performed using a 16-slice GE Lightspeed (n = 7) or single slice GE Prospeed (n = 1) helical scanner (General Electric Co., Milwaukee, Wisconsin) with a dual-phase (n = 3) or triple-phase (n = 5) technique. Dogs were placed under general anesthesia and scans were acquired at inspiration using a breath hold at 20 mm Hg. Angiographic studies were acquired by injecting 2.38 mL/kg of nonionic iodinated contrast medium (Isovue 370, Bracco Diagnostics Inc, Princeton, New Jersey) into a cephalic vein with a power injector (Vistron CT, Medrad Inc, Warrendale, Pennsylvania) at a rate of 5 ml/kg (body weight >10 kg) or hand injection (body weight < 10 kg). Timing delays were determined by a test bolus using 0.5 mL/kg of contrast medium under the same injection con- ditions and dynamic CT scans with slice thickness of 5 mm, identical kV and mA settings to the angiographic scan, and rotation time of 1 s for 60 s. Noncontrast and angiographic images were acquired in helical mode with 120 kV, 100-200 mA, and 0.625-3.0 mm slice thickness with soft tissue recon- struction algorithm. A standard soft tissue window (350 HU) and level (40 HU) were adjusted to maximize the conspicuity of the adrenal tumor and thrombus.
In all dogs that underwent a CECT scan, tumor volume of the largest adrenal mass was calculated using a commer- cially available imaging analysis software package (OsiriX, v6.0 64 bit, Pixmeo, Bernex, Switzerland) and recorded as total tumor volume. The maximal diameter of the tumor and maximal length and width of the segment of the tumor thrombus within the vena cava (not including the component within the PAV) was measured by a board certified radiolog- ist (AZ) using 3D multiplanar reconstruction to optimize the visibility of the thrombus. The radiologist was blinded to the surgical findings. The maximal width of the PAV at its point of insertion into the vena cava was also measured (Figure 1).
2.3 Patient preparation and anesthesia |
In cases where a functional tumor had been diagnosed or was suspected based on preoperative diagnostic evaluation, pretreatment with either Trilostane (for dogs with concurrent hyperadrenocorticism) or phenoxybenzamine (for those sus- pected to have pheochromocytoma) was administered for 2-3 weeks preoperatively. Dogs were placed under anesthesia on the day of surgery using a nonstandardized protocol chosen at the discretion of the attending anesthesiologist. Dogs were prepared for surgery by clipping hair from the ventral abdo- men from the mid-thoracic level to the mid-pelvis and later- ally to the upper third of the abdominal wall on each side, allowing for a paracostal incision to be performed should that have been deemed necessary. The ventral abdomen was aseptically prepared for surgery. Direct blood pressure, pulse oximetry, blood gas analysis, and measurement of end-tidal
A
B
C
carbon dioxide concentration were performed for routine anesthetic monitoring. Hypertension was defined as a sys- tolic blood pressure >180 mm Hg and hypotension was defined as systolic blood pressure <80 mm Hg.7
2.4 | Surgery
The peritoneal cavity was approached surgically through a ventral midline celiotomy extending from the xiphoid pro- cess to several centimeters cranial to the pubic brim. Upon entering the peritoneal cavity, the falciform fat was resected to enhance visualization. Balfour retractors were placed to provide access to abdominal organs and a full exploration of the abdominal cavity was performed in all dogs. Adrenal masses were isolated using a combination of blunt dissec- tion, hemoclips, and the use of electrosurgical devices until the mass was completely dissected and only attached to the vena cava by the PAV attachment. In all cases, monopolar electrosurgical probes were used and in some cases vessel- sealing devices (Force-Triad, Medtronic, Salem, Massachu- setts) were used to seal small bleeding vessels feeding the adrenal mass. In some dogs, Rummel tourniquets were pre- placed around the vena cava cranial and caudal to the tumor thrombus and around the renal veins but were not tightened in all dogs in which they were placed. Prior to removal of the tumor thrombus, a suture was preplaced but not tightened around the PAV at the point of its entry into the vena cava. When Rummel tourniquets were tightened to provide inflow occlusion to the affected segment of vena cava, this was done immediately prior to initiation of the phrenicoabdomi- nal venotomy. The venotomy was performed in a longitudi- nal fashion starting 3-4 mm from the point at which the PAV joined the vena cava with a number 11 scalpel blade (Figure 2). Once the vein had been incised, the tumor throm- bus, if present, was grasped with atraumatic forceps and gently withdrawn from the vena cava. As soon as the
tumor thrombus had been completely removed, the preplaced ligating suture was tied tightly to prevent any further hemor- rhage. This technique did not therefore involve any intentional incising of the vena caval wall or the need for any cavotomy repair. After removal of the tumor thrombus, remaining attach- ments of the adrenal mass were severed and the adrenal mass and tumor thrombus were removed en bloc and submitted for histopathological analysis. Ancillary procedures performed
in addition to adrenalectomy were recorded. Closure of the celiotomy incision was routine after copious sterile saline lavage of the peritoneal cavity had been performed.
2.5 | Outcome
Hospitalization time and all intraoperative and postoperative complications were recorded for each case. Medical records and telephone calls to the owners were used to establish out- come in each case. Follow-up time was reported.
3 RESULTS |
3.1 Animals |
Eight dogs met the criteria for inclusion in the study and underwent surgery between April 12, 2010 and December 9, 2016. There were 2 Shih Tzus and one each of English Springer Spaniel, Cocker Spaniel, Labrador Retriever, Jack Russell Terrier, Papillon, and mixed breed dog. Six were female spayed and 2 were male castrated. Median body weight was 9.9 kg (range, 5.4-25 kg). Median body condi- tion score was 6/9 (range, 4/9-9/9). Median age was 135 months (range, 96-168 months).
3.2 Preoperative evaluation |
Historical comorbidities were present in 4 dogs and included lymphosarcoma (n = 1), inflammatory bowel disease (1), uri- nary tract infection (1), diabetes mellitus (1), patella luxation (1), and hypothyroidism (1). Clinical signs at presentation included polydipsia with polyuria (n =2), pollakiuria (2), hematuria (1), polyphagia (1), lethargy (1), inappetence (1), diarrhea (1), vomiting (1), lethargy (1), and anxiety (1). Abnormalities detected on physical examination included the following: heart murmur (n = 3), thinning haircoat (2), hepa- tomegaly (3), subcutaneous masses (3), dental plaque (1), facial nerve paralysis (1), and cataracts (1). Results of com- plete blood counts and biochemical screens did not reveal any consistent or specific findings. The results of endocrine testing were consistent with pituitary-dependent hyperadre- nocorticism (n = 2), adrenal-dependent hyperadrenocorticism (1), or diabetes mellitus (1). Four dogs were not diagnosed with an endocrinopathy based on preoperative endocrine test- ing. One dog diagnosed with pituitary-dependent hyperadre- nocorticism (and a pheochromocytoma on histopathology) had an elevated urine normetanephrine:creatinine ratio (1433 ug/g, reference range, 28-380 µg/g) but a urine metaneph- rine:creatinine ratio that was within the normal range (109 ug/g, reference range, 18-359 µg/g). Two dogs had eleva- tions in serum Spec cPL concentrations preoperatively (600 and 620 µg/L, reference range, 0-200 µg/L). Blood pressure
was measured in 6 of 8 dogs preoperatively. Two of 6 dogs (both diagnosed with pheochromocytomas on histopathol- ogy) were found to be hypertensive preoperatively with a systolic blood pressure of 238 and 181 mm Hg, respectively. The remaining 5 dogs were in the normal range. All dogs were treated preoperatively with at least one medication. Six dogs were administered phenoxybenzamine (median dose 0.5 mg/kg, range, 0.4-0.8 mg/kg PO every 12 hours) for a minimum of 2 weeks preoperatively. Two dogs were treated with trilostane (dose: 0.4 and 1 mg/kg PO every 12 hours) for 4 weeks (a dog diagnosed with adrenal-dependent hyper- adrenocorticism) and 9 months (a dog diagnosed with pituitary-dependent hyperadrenocorticism) preoperatively. One dog was also being treated with prednisone (0.5 mg/kg PO every 12 hours for chronic management of inflammatory bowel disease), levothyroxine (0.02 mg/kg PO every 12 hours), and neutral protamine Hagedorn (NPH) insulin (0.5 units subcutaneously every 24 hours).
3.3 | Anesthesia
Complete anesthesia records were available for all dogs. Pre- medication for anesthesia was administered using a combina- tion of an opioid and an anticholinergic agent in most cases. Two dogs were administered methadone (0.1 mg/kg IV), 2 were administered oxymorphone (0.05-0.07 mg/kg IM or subcutaneously), 2 were administered hydromorphone (0.08- 0.1 mg/kg IM or subcutaneously), and 2 received morphine (1 mg/kg IM). Five dogs were administered atropine (0.02 mg/kg subcutaneously) and 1 received glycopyrrolate (0.01 mg/kg IV). Six dogs were induced by administration of combinations of fentanyl (median dose 8.3 mg/kg, range, 3.3-16 mg/kg IV) and midazolam (0.2 mg/kg IV) or diaz- epam (0.5 mg/kg IV). Two dogs were administered combina- tions of propofol (1.6-2 mg/kg IV) and either midazolam (0.2 mg/kg IV) or lidocaine (1.6 mg/kg IV). One dog was administered alfaxolone (0.65 mg/kg IV) in combination with fentanyl for induction. All dogs were administered isoflurane or sevoflurane in oxygen or were administered a continuous rate infusion of fentanyl for maintenance of anesthesia. Three dogs experienced hypertensive episodes during anesthesia (median systolic blood pressure 185-190 mm Hg). These epi- sodes were not treated with any specific medications. Of the 3 dogs with intraoperative hypertension, 2 had pheochromo- cytomas and 1 had an adrenocortical adenoma.
3.4 | Diagnostic imaging
All dogs underwent thoracic radiography prior to surgery. In 3 dogs, findings were within normal limits. Three dogs had mild left atrial enlargement, one of which had a heart murmur; an echocardiogram in this dog revealed mild mitral
| Dog number | Max tumor diameter (mm) | Tumor volume (cm3) | Max thrombus length (mm; caval component) | Max thrombus width (mm; caval component) | Max PAV width (mm; PAV-caval jct) | Ratio thrombus to PAV width |
|---|---|---|---|---|---|---|
| 1 | 11 | 1.2 | 24 | 10 | 8 | 1.2 |
| 2 | 25 | 11.4 | 10 | 7 | 3 | 2.3 |
| 3 | 20 | 5 | 6 | 4 | 4 | 1 |
| 4 | 14 | 2.3 | 11 | 8 | 3 | 2.7 |
| 5 | 20 | 5.4 | 12 | 3 | 3 | 1 |
| 6 | 18 | 13.5 | None present | None present | Not available | |
| 7 | 17 | 3.9 | 23 | 3 | 2 | 1.5 |
| 8 | 13 | 1.3 | 2 | 5 | 3 | 1.7 |
Abbreviations: Max, maximum; PAV, phrenicoabdominal vein.
and tricuspid valve degeneration and insufficiency. The 2 remaining dogs with heart murmurs did not undergo echocar- diographic examination. One dog had a small soft tissue opac- ity approximately 1 cm in diameter, which was not aspirated, and 1 dog had evidence of inflammatory lower airway disease.
All dogs underwent abdominal ultrasonography prior to surgery. Three dogs had left-sided adrenal masses and 4 had right-sided masses. One dog had bilateral adrenal masses. Two dogs were noted to have nodules/masses in the contra- lateral nonresected glands and 1 was described as having a small contralateral adrenal gland. At the time of abdominal ultrasonography, 6 of 8 dogs had evidence of PAV invasion by tumor thrombus and 4 of 8 had evidence of tumor thrombus extending into the vena caval. Other findings on abdominal ultrasound included polypoid cystitis (n = 2), cystitis (1), hepa- tomegaly (1), degenerative renal disease (1), mild common
common bile duct dilation (1), and portal vein thrombus (1). Ultrasound examination was performed a median of 20.5 (range, 1-83 days) days prior to CECT.
CECT scans were performed in all dogs and occurred on the day of surgery in 7 dogs and 3 days before surgery in 1 dog. Measurements of resected adrenal mass and associated tumor thrombus dimensions are summarized in Table 1. On CECT, the adrenal masses were located in the right adrenal gland in 4/8 dogs, and in the left adrenal gland in 4/8 dogs. Six of the 8 dogs had contralateral adrenal nodules/masses, one of which was also invading the PAV to a smaller degree than the larger mass (this dog was the only dog that under- went bilateral adrenalectomy). The resected adrenal masses had a median maximum diameter of 18 mm (11-25 mm) and a median volume of 4.4 cm3 (1.2-13.5 cm3). There was min- eralization of 4/8 lesions (Figure 3), with 2/4 involving the
*
*
A
B
Phrenicoabdominal Vein
Phrenicoabdominal Vein
Adrenal Mass
Thrombus
Vena Cava
Vena Cava
Adrenal Mass
A
B
Vena Cava
C
mass only (pheochromocytoma, carcinoma), 1/4 involving the mass and thrombus (adenoma), and 1/4 involving the thrombus only (carcinoma). The adrenal gland masses had mild to strong peripheral contrast enhancement in the arte- rial phase and heterogeneous enhancement in the portal phase images.
The invasion of the PAV was present between the ven- trolateral margin of the adrenal gland to the caudal vena cava in 7/8 dogs, and 1/8 dogs had no visible vascular invasion. The PAV containing thrombus was closely adhered to the capsule of the adrenal gland and was often indistinguishable from the mass where it remained in contact. Two of 8 dogs had extension of the mass dorsally in the PAV that did not reach the epaxial muscles.
The portions of the tumor thrombus in the caudal vena cava began at the widened PAV (median 3 mm, range, 2-8 mm) and extended a variable distance cranially (median 11 mm, range, 2-24 mm). The maximum width of the throm- bus (median 5 mm, range, 2-10 mm) was generally less than half of the diameter of the caudal vena cava and did not cause vascular obstruction. The dog without vascular invasion had a very large mass (13.4 cm3) that compressed the caudal vena cava as it contacted the caudal margin of the liver. In this case, there was some suspicion for PAV and vena caval inva- sion from ultrasound examination and so PAV venotomy was still pursued in order to rule out the presence of PAV and/or vena caval thrombus.
3.5 | Surgery
All dogs underwent ventral midline celiotomy and no dog required a paracostal incision (Figure 4). In 7 of 8 dogs, the Force Triad vessel-sealing device was used in addition to monopolar electrosurgery. Rummel tourniquets were pre- placed in the following fashion in 5 dogs: right renal vein and vena cava cranial and caudal to the thrombus (n = 3), vena cava cranial and caudal to thrombus (1), and right and left renal vein and vena cava cranial and caudal to thrombus
(1). In one of these dogs, Rummel tourniquets were placed but not actually tightened around the vena cava or renal veins around which they were placed. In the remaining 3 dogs, no Rummel tourniquets were placed. A Satinsky clamp was used to partially occlude the vena cava in 2 dogs to aid in limiting blood loss during thrombus resection. After thrombus removal, the PAV was ligated using 2 ligatures of 2-0 to 4-0 polydioxanone (n = 3), 2-0 to 5-0 polypropylene (2) or 3-0 silk (1). In 1 dog, a single ligature of 3-0 polydiox- anone was placed on the PAV. In 1 dog (with the largest vena caval tumor thrombus-dog 1 in Table 1), the phreni- coabdominal venotomy was lengthened into a cavotomy as fragmentation of the thrombus started to occur during removal. To repair the caval venotomy, a simple continu- ous closure using 5-0 prolene was used to close the defect in the wall of the vena cava. In 2 dogs, simple ligation of the PAV was supplemented by placement of one medium/ large hemoclip in 1 dog and placement of a horizontal mat- tress suture in the wall of the vena cava over the ligation site in a second dog. In all 7 dogs where tumor thrombus was present, complete removal of tumor thrombus was achieved. Additional procedures performed using standard techniques included liver biopsies (n =5), splenectomy (1), subcutaneous sarcoma resection (1), and bladder biopsy (1). In 2 dogs, transfusions were administered on the day of sur- gery in the following manner: packed red blood cells (1 unit in 1 dog and 2 units in a second dog), plasma (1 unit in 2 dogs). One of these 2 dogs also received 7 units of plasma on the second day after surgery, and the other received a further unit of packed red blood cells on the fourth postopera- tive day.
Median anesthesia time was 292 minutes (range, 210-360 minutes) and this included the time for CECT scanning in 7 of 8 dogs. Median surgical time for all dogs was 140 minutes (range, 80-225 minutes). Surgical time included the time to complete the adrenalectomy and the additional procedures that were performed at the time of celiotomy.
3.6 Histopathological details |
In the 7 dogs with unilateral adrenal masses that were resected, the histopathological diagnosis was pheochromocy- toma in 4 dogs, adrenocortical carcinoma in 2, and adreno- cortical adenoma in 1 dog. The dog with bilateral adrenal masses had a left-sided pheochromocytoma and a right-sided pheochromocytoma with focal adrenocortical adenoma. In 2 of the dogs diagnosed with pheochromocytoma, histopatho- logical evaluation of the portion of the mass that had invaded the PAV and vena cava revealed that it was entirely com- posed of tumor tissue and not thrombus. Liver biopsies har- vested from 6 dogs revealed mild or moderate vacuolar hepatopathy (n = 3), mild steroid hepatopathy (1), glycoge- nosis and lipogranulomas (1), and severe chronic vacuolar hepatopathy with periportal fibrosis (1). One dog underwent splenectomy and was diagnosed with mild multifocal eryth- ropoeisis. One dog had a bladder biopsy performed, which revealed lymphocytic, plasmacytic, and histiocytic cystitis. One was dog was diagnosed with a soft tissue sarcoma.
3.7 Postoperative care |
All dogs were recovered in an intensive care environment with 24-hour monitoring. Analgesia protocols were selected at the discretion of the attending clinicians. Patients received intermittent injectable opioids for 24 hours (hydromorphone [0.025-0.05 mg/kg q4 hours] or methadone [0.1-0.2 mg/kg q4 hours]). One dog administered methadone for 24 hours was switched to buprenorphine (0.01 mk/kg IV q6 hours) for a further 48 hours and was not discharged with any analgesic medication after 6 days in hospital. Five further dogs that were discharged from the hospital were administered trama- dol hydrochloride (2-5 mg/kg PO q8-12 hours) for 5-7 days.
3.8 Complications and outcome |
Intraoperative complications occurred in 1 dog. During attempted removal of the tumor thrombus through the phre- nicoabdominal venotomy site, it fragmented and the incision had to be extended 8 mm into the caudal vena cava to allow complete retrieval, which was achieved. Closure of the resulting defect in the caudal vena cava was performed by placement of a continuous line of simple continuous 5-0 polypropylene. This patient was the patient with the largest thrombus and significant distension of the PAV (8 mm). In the same dog, marked congestion of the jejunum and ileum was noted intraoperatively along with the presence of poor mesenteric arterial pulse quality. This appeared to persist for approximately 30-40 minutes and appeared to resolve after adrenal resection was complete. The origin of this congestion was unknown.
Two dogs died in the perioperative period. The dog in which congestion in the jejunum and ileum was visualized during surgery suffered cardiopulmonary arrest 1 day postoperatively and owners elected euthanasia without resus- citation. A second dog developed severe pancreatitis and bronchopneumonia and owners elected euthanasia on the sixth postoperative day. The remaining 6 dogs were dis- charged from the hospital. Median hospital stay for these 6 dogs was 5 days (range, 2-7 days). Median number of post- operative hours in hospital was 75 (range, 27-120 hours).
Owners of 6 dogs that survived to discharge were con- tacted by telephone to obtain long-term follow-up. All 6 remain alive at the time of follow-up a median of 14.5 months (range, 1-55 months) postoperatively. One dog that had an adrenocortical carcinoma resected underwent a recheck ultrasound examination at 3 months postoperatively. Mesenteric lymphadenopathy was detected and an aspirate of the lymph node was performed, which revealed carcinoma cells most likely of adrenal origin. No specific therapy was initiated. At 10 months postoperatively, a second abdominal ultrasound was performed, and revealed further progression of the mesenteric lymphadenopathy but the dog was still doing very well. This dog remains alive and doing well 17 months postoperatively.
4 DISCUSSION |
This study describes a modification of the traditional tech- nique for tumor thrombectomy in dogs with invasive adrenal masses. In a subsection of dogs with either small tumor thrombi or those with significant PAV distension, it is possi- ble to make the incision required to remove the caval compo- nent of the tumor thrombus in the PAV instead of the vena cava, thus obviating the need for a cavotomy entirely. The study describes the technique in 8 dogs with no control pop- ulation that could be used for comparison and so no firm comparisons can be drawn from these limited data as to whether this technique is in any way superior in this case population. The authors hypothesize, however, that this tech- nique may simplify the removal of tumor thrombi and could possibly help to reduce blood loss and perioperative morbid- ity in this patient population. The small number of dogs reported in this study cannot be compared to any historical controls as if any of the dogs in previous studies were treated by PAV vein incision, it was not reported, and no previously published studies report clinicopathological data or outcome on dogs with small thrombi such as those present in the majority of dogs in this study. Degree of tumor thrombus extension has been previously reported to be prognostic in dogs, and so the dogs in this study might be expected to have better outcomes than those with caval thrombi extend- ing into the hepatic vena cava.5 Despite not having any
intraoperative mortality in this cohort of 8 dogs, 2 dogs did die from complications in the postoperative period prior to dis- charge from the hospital, and this is testament to the ongoing challenges inherent in management of these complex cases.
Case selection for the approach used on the dogs in this report is likely to be largely based on the findings of diag- nostic imaging. Ultrasound examination of these lesions only reported vena caval tumor thrombus in 4 of 8 cases, although it should be noted that a median lag time of 20.5 days occurred between the ultrasound examination and the CECT scan being performed. In 1 dog, no PAV or vena caval thrombus was found either on CECT or at the time of sur- gery. It is difficult to say whether the ultrasound examina- tions failed to detect caval thrombi in the remaining 3 dogs or whether the vascular invasion occurred in the time lag between ultrasound and CECT being performed in these dogs. It has been shown previously that ultrasound has lower sensitivity compared to CECT in detection of tumor thrombi, but it is unclear whether the results of this study lend support to those data or not because of the lack of contemporaneous imaging in these cases.4,8 The authors suggest that the key to the use of a phrenicoabdominal venotomy for removal of caval tumor thrombi is the presence of a modestly sized thrombus whose maximal width does not greatly exceed the width of the PAV at its entry point into the vena cava. If such a discrepancy were present, the vena caval thrombus would presumably lodge at the entrance to the PAV and resist being pulled through the venotomy site, or perhaps start to fragment. This happened in one case in this series, necessitating extension of the phrenicoabdominal venotomy into the vena cava to avoid further fragmentation, which could lead to thromboembolism. Interestingly, in most dogs in this series the maximal width of the caval component of the tumor thrombus did somewhat exceed the maximal width of the PAV at its point of entry into the vena cava (Table 1). It therefore seems possible for tumor thrombi slightly wider in diameter than the PAV width to be removed through the PAV venotomy technique although the maximal PAV width to thrombus width ratio that will result in safe and reliable caval thrombus retrieval through this technique cannot be inferred from such a small case series. From our cases, we can see that the case with the largest discrepancy had a maxi- mal thrombus width of 8 mm with a PAV width of no more than 3 mm (maximal thrombus width to PAV width ratio of 2.7). In the remaining dogs, the discrepancy was not as large. The effect of length of the caval component of tumor throm- bus on success of this technique is also unknown. In 1 dog in this cohort, a very narrow (3 mm width) but long caval thrombus (23 mm in length) could easily be retracted into the PAV for complete removal without excessive traction needing to be applied and without any fragmentation occur- ring. It is, however, possible that if this study contained a
larger cohort of dogs with longer tumor thrombi that more complications with thrombus fragmentation could be seen, and future studies with larger numbers of cases should be performed to further evaluate this question.
The surgical technique was completed reasonably consis- tently in this case cohort although some variation occurred. In all cases and in common with most reports in the litera- ture, the adrenal mass was dissected free from all surround- ing structures prior to embarking on retrieval of the tumor thrombus from the PAV and vena cava. In cases in this report, the decision to proceed with a PAV incision instead of a cavotomy was made prior to surgery and was based on the dimensions of the tumor thrombus and PAV geometry as has been discussed. In 5 of the 8 dogs, Rummel tourniquets were preplaced around the vena cava and, in some cases, the renal veins in order to obtain inflow occlusion to the affected segment of vena cava prior to venotomy. The placement of Rummel tourniquets does not take a great deal of additional time and may facilitate hemorrhage control in cases where unforeseen complications may be encountered, such as the case with a large vena caval thrombus in this case series. However, in the 3 cases where Rummel tourniquets were not placed, and in the 1 dog where tourniquets were placed but not tightened prior to phrenicoabdominal venotomy, the sur- geons felt that occluding vena caval flow was not necessary. None of these cases experienced hemodynamically signifi- cant blood loss and none were treated with blood or plasma transfusions. These were all cases in which small thrombi were present. The authors have found that with preplacement of the encircling suture around the PAV, little hemorrhage generally occurs between the time that the phrenicoabdomi- nal venotomy is made, the tumor thrombus is removed, and the preplaced suture is tightened, thereby preventing further blood loss. After the venotomy has been made, the presence of the thrombus itself tends to tamponade hemorrhage until the time that it has been removed through the venotomy site limiting hemorrhage to the time between thrombus removal and suture tightening. This is likely also the reason why in only 2 cases Satinsky clamps were used for partial occlusion of the vena cava during venotomy. A cavotomy incision can take some minutes to close and so partial occlusion can be very helpful in minimizing blood loss during closure, but tightening the preplaced ligature on the PAV is very rapid and so in most cases partial occlusion using a Satinsky clamp was not felt to be necessary.
There are significant limitations to this study. Only a small number of cases are reported and given a larger cohort of patients, conclusions regarding outcomes in comparison to alternative techniques for tumor thrombectomy might be dif- ferent. The cases in this cohort did not have uniform pathol- ogy and multiple surgeons performed the surgeries using slightly different techniques. The heterogeneity of these
factors makes drawing firm conclusions regarding the tech- nique challenging.
In conclusion, the authors believe that this procedure deserves its place in the armamentarium of techniques for surgical management of invasive adrenal neoplasia. Although not proven by the data in this study, it is hypothe- sized that in the small subset of dogs with invasive adrenal neoplasia that have small caval tumor thrombi or significant distension of the PAV that phrenicoabdominal venotomy might provide some advantages over cavotomy.
CONFLICT OF INTEREST
The authors declare no conflicts of interest related to this report.
ORCID
Allison L. Zwingenberger ®http://orcid.org/0000-0002- 8982-2558
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How to cite this article: Mayhew PD, Culp WTN, Balsa IM, Zwingenberger AL. Phrenicoabdominal venotomy for tumor thrombectomy in dogs with adrenal neoplasia and suspected vena caval invasion. Veterinary Surgery. 2017;00:000-000. https://doi.org/10.1111/vsu. 12728