Introduction
Apocrine gland anal sac adenocarcinoma (AGASACA) is the result of the neoplastic transformation of glandular epithelial cells of the apocrine gland of the anal sac.1–3 AGASACA is considered a locally invasive and highly metastatic disease.1–4 The presence of metastasis is often detected at the time of initial anal sac mass diagnosis, and it is most commonly detected at the iliosacral lymph center before reaching distant sites like abdominal organs or the lungs.1,5,6
The definitive treatment for AGASACA often involves anal sacculectomy and extirpation of any metastatic iliosacral lymph nodes.3 Both chemotherapy and radiation therapy are recommended adjunct treatments, and closed and open techniques for anal sacculectomy have been described.3 The open approach, which involves making a direct incision into the anal gland to expose the lining of the anal sac, is considered faster and simpler to perform but inappropriate for anal sacs affected by tumors.7 The closed technique keeps the anal sac completely intact, therefore decreasing contamination of surrounding tissue and the potential for postoperative infection.7,8 The closed technique is recommended for anal sacculectomy for neoplasia.8 A potential drawback to the use of the traditional closed technique is that the anal sac duct is not fully excised but only ligated. A modified approach to the closed anal sacculectomy has been described to facilitate full anal sac duct excision with minimal surrounding soft tissue trauma by use of a hemostat to assist with intraoperative manipulation and traction of the anal sac.9 Minimal short-term complications were reported with the procedure.9 No long-term outcomes, including recurrence or metastasis rates, have been reported following the use of this modified closed technique for dogs with anal sac neoplasia.
The objective of this study was to report the short-term and long-term outcomes, recurrence, and metastasis rates of dogs that underwent the modified closed anal sacculectomy or traditional closed anal sacculectomy for treatment of anal sac neoplasia. The authors hypothesized that dogs that received the modified closed approach would have lower recurrence rates and fewer short-term and long-term complications than the traditional closed approach.
Methods
Case selection criteria
The electronic medical records of The Ohio State University College of Veterinary Medicine and the University of Illinois College of Veterinary Medicine were searched to identify dogs with a histopathologic diagnosis of AGASACA that underwent anal sacculectomy surgery with either the traditional closed or modified closed technique between January 1, 2016, and December 31, 2020. Search terms included anal sacculectomy, anal sac mass, and anal sac neoplasia. To be included in the study, dogs were required to have undergone preoperative imaging (abdominal ultrasound [AUS], CT, or thoracic radiographs [CXR]); complete preoperative physical examination, surgery, and histological examination reports; and ≥ 250 days of clinical follow-up. Dogs that died before the minimum 250-day follow-up period were included in the study. Follow-up was performed by 2 investigators (GSF and JMT) with the referring veterinarian if there was no documented examination at the contributing institution ≥ 250 days following surgery. Owner follow-up via email or telephone was attempted if data were not available from the referring veterinary clinic. Dogs were excluded from the study if the anal sacculectomy surgery was performed for nonneoplastic disease, an open anal sacculectomy was performed, or the dog was lost to follow-up < 250 days following surgery.
Medical records review
Data collected from the medical records included signalment and examination findings at the time of initial presentation, results of any preoperative laboratory analyses, and abnormal results of diagnostic imaging or other diagnostic tests (eg, fine-needle aspiration and cytology) if applicable. Any perioperative treatments, antimicrobial, and neoadjuvant therapy (including radiation therapy and chemotherapy) administered were recorded.
The anesthesia and surgery records were reviewed, and the type of anal sacculectomy performed, traditional or modified, was classified on the basis of previously reported procedure descriptions.9,10 The laterality of anal sacculectomy and concurrent procedures that were performed were noted. Histological examination findings of excised tissue and any postoperative treatments were recorded.
A complication was defined as any adverse event associated with the preoperative time period (before surgical intervention), intraoperative time period (the time of skin incision to skin closure), or postoperative time period (after skin closure).11 Any intraoperative and postoperative complications were evaluated and graded retrospectively via medical record review. Intraoperative complications were graded (from 0 [no deviations from the ideal surgical course] to IV [intraoperative death]) by use of the Classification of Intraoperative Complication System.12 Postoperative complications were graded (from 0 [minimal complications] to 4 [postoperative death]) by use of the Contracted Accordion Severity Classification system.13 Postoperative complications were categorized as short-term (from the time of hospitalization to recheck examination 10 to 14 days following surgery) or long-term (the time period following recheck examination).
Local recurrence was suspected by either physical examination (digital rectal palpation) or confirmed with diagnostic testing (fine-needle aspiration and cytology, histopathology, or CT). Confirmed metastatic disease was determined with recheck of thoracic diagnostic imaging (CT or CXR), or abdominal diagnostic testing (fine-needle aspiration and cytology or histopathology). Suspected metastatic disease was determined with abdominal imaging (CT or AUS) but without cytological or histopathological confirmation.
Statistical analysis
Descriptive statistics were calculated to summarize dog signalment information at the time of surgery. Continuous variables were assessed for normality with Shapiro-Wilk tests. Normally distributed data were reported as mean ± SD, and nonnormally distributed data were reported as median and IQR. Time to local recurrence was calculated as the number of days from the date of surgery to the date of detected local recurrence. Time to metastasis was calculated as the number of days from the date of surgery to the date of detected metastasis, either confirmed or suspected. The median duration of follow-up was calculated as the number of days from the date of surgery to the date of death, euthanasia, or last follow-up. Survival time was calculated as the number of days from initial diagnosis to the date of death or euthanasia. Complication rates and recurrence proportions were compared using Fisher exact tests. Factors with a P value < .05 were considered significant for all comparisons. All statistical analyses were performed using statistical software (SAS version 9.4; SAS Institute Inc).
Results
Dogs
A total of 137 dogs that underwent anal sacculectomy were initially identified following an electronic medical record search. Of these, 47 dogs were excluded from the statistical analysis. Reasons for exclusion included the following: incomplete medical records (n = 21), surgery was performed for nonneoplastic disease (12), loss to follow-up (6), an open anal sacculectomy was performed (4), and duplicate records (4).
Thirty-five dogs were identified that had a modified closed anal sacculectomy performed and met the inclusion criteria. Of the 35 dogs, 22 (62.9%) dogs were treated at The Ohio State University College of Veterinary Medicine and 13 (37.1%) dogs were treated at the University of Illinois College of Veterinary Medicine. Fifty-five dogs were identified that had a traditional closed anal sacculectomy and met the inclusion criteria. Of the 55 dogs, 36 (65.5%) and 19 (35.5%) dogs were treated at The Ohio State University College of Veterinary Medicine and the University of Illinois College of Veterinary Medicine, respectively. Dog demographics by procedure (modified or traditional closed anal sacculectomy) are presented (Table 1).
Patient demographics including median age, weight, and body condition score; sex; and breed of dogs presenting for a closed (modified or traditional) anal sacculectomy.
| Demographic | Total | Modified | Traditional |
|---|---|---|---|
| Age (y) | |||
| Median (range) | 10.2 (9.7) | 11.02 (9.7) | 10.1 (8.7) |
| Weight (kg) | |||
| Median (range) | 24.8 (51.3) | 23.2 (37.2) | 25.5 (51.2) |
| Body condition score (1–9) | |||
| Median (range) | 5 (6) | 6 (5) | 5 (6) |
| Sex | |||
| Intact female | 0 | 0 | 0 |
| Spayed female | 16 | 9 | 7 |
| Intact male | 2 | 0 | 2 |
| Neutered male | 72 | 26 | 46 |
| Breed | |||
| American Staffordshire Terrier | 1 | 0 | 1 |
| Australian Shepherd | 2 | 1 | 1 |
| Basset Hound | 1 | 0 | 1 |
| Beagle | 2 | 0 | 2 |
| Border Collie | 3 | 2 | 1 |
| Cavalier King Charles Spaniel | 1 | 1 | 0 |
| Cocker Spaniel | 1 | 1 | 0 |
| Coton de Tulear | 1 | 1 | 0 |
| Dachshund | 2 | 0 | 2 |
| English Bulldog | 1 | 0 | 1 |
| Flat Coated Retriever | 1 | 0 | 1 |
| German Shepherd Dog | 3 | 0 | 3 |
| Golden Retriever | 3 | 3 | 0 |
| Labrador Retriever | 6 | 1 | 5 |
| Lhasa Apso | 1 | 0 | 1 |
| Maltese | 3 | 1 | 2 |
| Miniature Dachshund | 1 | 1 | 0 |
| Miniature Schnauzer | 3 | 1 | 2 |
| Rhodesian Ridgeback | 1 | 0 | 1 |
| Sheltie | 1 | 0 | 1 |
| Shetland Sheepdog | 1 | 1 | 0 |
| Siberian Husky | 1 | 0 | 1 |
| Springer Spaniel | 3 | 1 | 2 |
| Standard Dachshund | 1 | 0 | 1 |
| Standard Poodle | 1 | 1 | 0 |
| Toy Poodle | 1 | 0 | 1 |
| Vizsla | 1 | 0 | 1 |
| Weimaraner | 1 | 0 | 1 |
| Welsh Springer Spaniel | 1 | 1 | 0 |
| Yorkshire Terrier | 1 | 1 | 0 |
| Mixed-breed dog | 40 | 17 | 23 |
| Institution | |||
| Illinois | 32 | 13 | 19 |
| Ohio | 58 | 22 | 36 |
Clinical findings
Modified closed anal sacculectomy group—Thirty-four dogs had unilateral, palpable anal sac masses (19 left-sided and 15 right-sided), and 1 dog had bilateral disease. The median maximum dimension of the anal sac mass found on physical examination was 2 cm (IQR, 5.8; range, 0.2 to 6 cm). Twenty had fine-needle aspiration and cytologic examination of the anal sac mass performed, and all but 2 had findings consistent with carcinoma. These 2 provided diagnoses of inflammation and basilar epithelial neoplasm.
All dogs had preoperative laboratory analysis (CBC, chemistry profile, or venous blood gas) performed, and 4 dogs had hypercalcemia (elevated total calcium). All dogs underwent diagnostic imaging for staging purposes before surgery, including CT alone (n = 14), AUS and CXR (6), CT and AUS (1), and CT and CXR (14). Six dogs had aspirates of their enlarged iliosacral lymph nodes, which confirmed metastatic disease.
Six dogs had additional aspirates performed on other organs (liver and spleen), and 3 dogs had additional aspirates performed on nonregional lymph nodes (mandibular, periaortic, and popliteal). No dogs had evidence of metastatic disease identified in these organs or lymph nodes.
Twelve dogs had a history of antimicrobial use (within 30 days prior to surgery), and none underwent neoadjuvant therapy before surgery (within 30 days prior to surgery).
Traditional closed anal sacculectomy group—Fifty-one dogs had unilateral, palpable anal sac masses (28 left-sided and 23 right-sided), and 4 dogs had bilateral disease. The median maximum dimension of the anal sac mass found on physical examination was 3 cm (IQR, 9.7; range, 0.3 to 10 cm). Thirty-five had fine-needle aspiration and cytologic examination of the anal sac mass performed, and all had findings consistent with carcinoma.
All dogs had preoperative laboratory analysis (CBC, chemistry profile, or venous blood gas) performed, and 12 dogs had hypercalcemia (elevated total calcium). All dogs underwent diagnostic imaging for staging purposes before surgery, including AUS alone (n = 6), CT alone (19), AUS and CXR (20), CT and AUS (1), CT and CXR (6), and all 3 modalities (3). Sixteen dogs had aspirates of the iliosacral lymph nodes following diagnostic imaging, which confirmed metastatic disease in all but 1 dog.
Fourteen dogs had additional aspirates performed on other organs (liver, lung, and spleen), and 2 dogs had additional aspirates performed on nonregional lymph nodes (prescapular and popliteal). Of those 14 dogs, 3 had evidence of metastatic disease (lung, n = 1; and spleen, 2). Nine dogs had a history of antimicrobial use (within 30 days), and none underwent neoadjuvant therapy before surgery (within 30 days).
Surgery—All 90 dogs underwent surgical excision of the primary mass, which included anal sacculectomy. The choice of modified versus traditional closed method was surgeon preference. All procedures were performed by an American College of Veterinary Surgeons board-certified surgeon or a trainee under direct supervision.
Modified closed anal sacculectomy group—Thirty-five dogs underwent the modified closed anal sacculectomy procedure. In 16 dogs, at least 1 additional surgical procedure was performed during the same anesthetic episode. Half of these dogs (n = 8) had iliosacral lymph node extirpation performed. Aside from lymph node extirpation, other surgical procedures performed included mass removal (n = 6), liver lobectomy (1), unilateral total ear canal ablation and bulla osteotomy (1), central hepatic mass microwave ablation (1), and unilateral kidney omentalization (1). Intraoperative complications were seen in 3 (8.6%) dogs. Five (14.3%) dogs had minor postoperative complications that resolved with medical management. Medical management included open wound management (n = 3), physical therapy following nonambulatory paresis suspected to be secondary to epidural administration (1), discontinuation of prescribed nonsteroidal anti-inflammatory medication (1), and administration of an antimicrobial (1). Adjuvant treatment, chemotherapy IV or PO, was pursued in 16 (45.7%) dogs. Dog intra- and postoperative outcomes by procedure (modified or traditional closed anal sacculectomy) are presented (Table 2).
Dogs presenting for anal sacculectomy technique, by technique performed (modified or traditional) that had intra- and postoperative complications, local recurrence, and postoperative metastatic disease. The median (range) of survival for dogs is presented as well.
| Variable | Total | Modified | Traditional |
|---|---|---|---|
| Intraoperative complications (No. of dogs [%]) | 10 | 3 (8.6%) | 7 (12.7%) |
| Postoperative complications (No. of dogs [%]) | 17 | 5 (14.3%) | 12 (21.8%) |
| Local recurrence of tumor (No. of dogs) | |||
| Confirmed | 16 | 8 (22.9%) | 8 (14.6%) |
| Suspected | 9 | 3 (8.6%) | 6 (10.9%) |
| Postoperative metastatic disease (No. of dogs [%]) | |||
| Confirmed | 22 | 8 (22.9%) | 14 (26.4%) |
| Suspected | 11 | 4 (11.4%) | 7 (13.2%) |
| Survival (No. of dogs [%]) | |||
| Alive | 63 | 22 (62.9%) | 41 (74.6%) |
| Dead | 27 | 13 (37.1%) | 14 (25.5%) |
| Survival (days) | |||
| Median (range) | 580 (4,224) | 536 (4,183) | 618 (1,628) |
Traditional closed anal sacculectomy group—Fifty-five dogs underwent the traditional closed anal sacculectomy procedure. In 39 dogs, at least 1 additional procedure was performed during the same anesthetic episode. Twenty-nine of these dogs had iliosacral lymph node extirpation performed. Aside from lymph node extirpation, other surgical procedures performed included mass removal (n = 5), cystotomy (3), splenectomy (3), liver lobectomy or biopsy (2), castration and scrotal ablation (1), internal obturator transposition for a perineal hernia (1), hemimandibulectomy (1), and unilateral exenteration (1). Intraoperative complications were seen in 7 (12.7%) dogs. Twelve (21.8%) dogs had minor postoperative complications that resolved with medical management. Medical management included administration of an antimicrobial (n = 3), open wound management (3), monitoring (2), administration of an anxiolytic (1), hospitalization for regulation of previously diagnosed diabetes mellitus (1), hospitalization for medical management of postoperative pancreatitis (1), and abdominal incisional closure revision following iatrogenic abdominal hernia formation (1). Adjuvant treatment was pursued in 33 (60%) dogs. Of these dogs, 31 received chemotherapy IV or PO and 2 received palliative radiation therapy treatment.
Histologic diagnosis
Modified closed anal sacculectomy group—Thirty-four dogs had a histologic diagnosis of AGASACA, and 1 dog had a diagnosis of a collision tumor composed of AGASACA and soft tissue sarcoma. All 8 dogs that had iliosacral lymph node extirpation at the time of anal sacculectomy had evidence of metastatic disease in these tissues on histologic examination.
Traditional closed anal sacculectomy group—All 55 dogs had a histologic diagnosis of AGASACA. Two dogs that received a bilateral anal sacculectomy were diagnosed with AGASACA in only 1 anal sac, with the other receiving a histological diagnosis of anal sacculitis. All 29 dogs that had iliosacral lymph node extirpation at the time of anal sacculectomy had evidence of metastatic disease in these tissues on histologic examination.
Long-term and clinical outcomes—Short-term and long-term outcomes by procedure (modified or traditional closed anal sacculectomy) are presented (Table 2).
Modified closed anal sacculectomy group—Tumor recurrence was confirmed in 8 (22.9%) dogs. Local recurrence was confirmed with fine-needle aspiration and cytology (n = 7) or CT (1). Local recurrence was suspected following digital rectal palpation in 3 (8.6%) dogs. Confirmed metastatic disease was reported in 8 (22.9%) dogs. Of these 8 dogs, thoracic metastatic disease was confirmed with CXR (n = 1) and CT (1), and abdominal metastatic disease was confirmed with fine-needle aspiration and cytology of the iliosacral lymph nodes (5) and liver and spleen (1). Suspected metastatic disease was reported in 4 (11.4%) dogs. Of these 4 dogs, abdominal metastatic disease was suspected following iliosacral lymph node enlargement visualization with AUS (n = 3) or CT (1). Twenty-two (62.9%) dogs survived to the 250-day follow-up period. The 1-, 2-, and 3-year survival rates were 68%, 49%, and 21%, respectively.
Traditional closed anal sacculectomy group—Tumor recurrence was confirmed in 8 (14.6%) dogs. Local recurrence was confirmed by fine-needle aspiration and cytology (n = 5), histopathology following surgical revision (2), or CT (1). Local recurrence was suspected following digital rectal palpation in 6 (10.9%) dogs. Confirmed metastatic disease was reported in 14 (26.4%) dogs. Of these 14 dogs, thoracic metastatic disease was confirmed with CXR (n = 7) and iliosacral lymph node metastatic disease was confirmed with fine-needle aspiration and cytology (5) and histopathology following surgical excision (2). Suspected metastatic disease was reported in 7 (13.2%) dogs. Of these 7 dogs, abdominal metastatic disease was suspected following iliosacral lymph node enlargement visualization with AUS (n = 5) or CT (2). Forty-one (74.6%) dogs survived to the 250-day follow-up period. The 1-, 2-, and 3-year survival rates were 81%, 49%, and 30%, respectively.
Comparisons between groups—No statistically significant difference in recurrence rate was noted between groups (P = .68).
Discussion
This study was the first to report the long-term outcomes associated with performing the modified closed anal sacculectomy technique for anal sac neoplasia. Before this, only 1 study9 had reported outcomes associated with the procedure, but clinical follow-up was a minimum of 30 days, which limits its utility for predicting long-term outcomes associated with the modified procedure. The aforementioned study highlighted several short-term advantages to performing the procedure, including controlled manipulation of tissue during dissection, minimal manipulation of adjacent soft tissue, and full excision of the gland and its associated duct.9 This study found no long-term advantage to performing the modified technique as opposed to the traditional technique, with respect to complication rate or local recurrence.
AGASACA commonly occurs in middle-aged to older dogs with a median age of 9 to 11.5 years of age (range, 5 to 15 years).2,3,9,14 The median age of this study population (10.2 years) is consistent with previously reported age ranges. While early studies suggested an increased proportion of neutered female dogs affected with AGASACA, sex and neuter status are no longer considered risk factors for the incidence of AGASACA.2,3,14–16 Neutered males were largely overrepresented (80%) in the current study population. A prior study15 documented that neutered males are more commonly affected than intact males, suggesting that the loss of hormones is associated with an increased incidence of neoplastic disease. A larger cohort of dogs with AGASACA needs to be examined to see whether this sexual dimorphism exists.
A closed anal sacculectomy technique is the recommended standard of surgical care because dogs are 13.76 times more likely to develop long-term complications following open anal sacculectomy.8 A prior study9 presented a modified technique for the closed anal sacculectomy and concluded that the procedure was well tolerated in dogs. In this study, the traditional and modified techniques were compared to determine whether one method provided lower complication rates compared to the other. Previously, intra- and postoperative complication rates for the traditional closed anal sacculectomy procedure have been reported as low as 1.8% and as high as 20%.3,4,8,17 In this study, intraoperative and postoperative complications were reported in 12.7% and 21.8% of dogs that underwent the traditional approach. The intraoperative and postoperative complication rates were similarly moderate in dogs that underwent the modified approach (8.6% and 14.3%). No significant difference in complication rates between the 2 groups was found. With either technique, the anal sacculectomy procedure is considered a contaminated one due to the incision’s proximity to the rectum. The radial incision required for the modified approach is generally closer to the rectum than the circumferential inaction used when performing the traditional approach. Despite this increased risk of infection, the modified group did not have higher surgical dehiscence or infection rates than the traditional group. A theoretical complication associated with performing the modified technique is increased external anal sphincter incision size secondary to duct removal. This ultimately was not the case in this group of dogs, as none of them were reported to experience postoperative fecal incontinence. Several dogs in this study suffered adverse events secondary to either anesthesia, a previously diagnosed comorbidity, or an additional surgical procedure performed during the same anesthetic event. A prospective study is warranted to reassess measurable outcomes (ie, surgery time and intraoperative and postoperative complication incidence) when anal sacculectomy is the only surgical procedure performed.
The goal of anal sacculectomy for a neoplastic disease is to provide local control of the disease.3,17–19 In this study, there was no advantage concerning local recurrence, metastasis, or survival with the modified closed anal sacculectomy technique. Prior studies have shown recurrence rates of 5% to 21% with the traditional closed anal sacculectomy procedure.9,19,20 As the modified and traditional closed anal sacculectomy procedures are both marginal excision procedures, the lack of difference in local recurrence between the 2 groups is not surprising. This study would support the idea that leaving a portion of the duct behind when performing the traditional approach does not lead to an increased recurrence rate. Complete removal of the duct did not increase survival time despite achieving larger surgical margins.
In this study, the assessment of the effect of adjuvant treatment on survival outcomes was limited due to the variations in disease burden and management and the difference in the standard of care between the 2 participating institutions. Three dogs in the traditional closed group had documented metastatic disease distant to regional nodes at diagnosis but were included in the analysis. Not all dogs in this study had owners that pursued adjuvant therapy. Additionally, not all dogs that had evidence of progressive metastatic disease pursued additional treatment. These factors could alter the metastasis rates and median survival time between study participants and should be strongly considered when interpreting differences in long-term outcomes between the 2 treatment groups.
Aside from variations in disease burden and management among dogs, other limitations existed within the current study. Only 90 dogs were identified for enrollment. A study with a larger cohort of dogs with increased statistical power could potentially identify a smaller statistical significance between the groups. The lack of longer-term formal veterinary follow-up for every dog in this study could have influenced recurrence and metastasis rates. About half of the dogs in this study population lacked clinical follow-up at the institution where surgery was performed, and a follow-up call to the owner or referring veterinarian was needed. Because the pursual of diagnostic testing and return doctor follow-up is at the discretion of the owner, local recurrence or metastasis could have gone undetected in some dogs. We attempted to lessen the impact of this limitation by separating local recurrence and metastasis cases into confirmed and suspected cases. Additionally, because of the study’s retrospective nature, intraoperative and postoperative complications could not be attributed to the anal sacculectomy procedure alone, potentially falsely increasing complication rates due to anesthetic or other concurrent surgical procedure complications.
In conclusion, the traditional and modified closed anal sacculectomy techniques resulted in moderate rates of recurrence of AGASACA. No long-term benefits were identified when performing the modified closed approach as opposed to the traditional closed anal sacculectomy technique. The results support surgeon preference in choosing a technique for anal sacculectomy for neoplastic disease. A clinical evaluation is warranted to assess whether the modified technique decreases contamination of surrounding tissue and the potential of postoperative infection when the procedure is performed for other anal sac diseases, such as chronic anal sacculitis, recurrent impaction, and anal sac abscess.
Acknowledgments
None reported.
Disclosures
Presented in part at the Veterinary Cancer Society and Veterinary Society of Surgical Oncology 2023 Collaborative Conference, April 20, 2023.
No AI-assisted technologies were used in the generation of this manuscript
Funding
The authors have nothing to disclose.
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