Advancements in surgical techniques, instrumentation, neoadjuvant chemo-radiotherapy, and immunotherapy have significantly enhanced sphincter preservation rates and reduced local recurrence rates for rectal cancer [11]. Nonetheless, patients with low or very low rectal cancer, where tumors are situated less than 5 cm from the anal verge, often require abdominoperineal resection to achieve safe surgical margins.
Introduced by Schiessel et al in 1994 [1], ISR has gained worldwide recognition as a safe and ultimate sphincter-sparing technique for a subset of very low rectal cancers due to stringent indication criteria, surgical technique advancements, and involvement of multimodal treatment [3, 4, 12–15]. However, the functional outcomes associated with sphincter-sparing surgeries for low rectal cancer patients remain suboptimal. Patients frequently experience compromised anal function postoperatively, characterized by difficulties in control, urgency, increased frequency of defecation, and fecal incontinence. These symptoms collectively constitute what is known as LARS [16]. For ISR surgery, postoperative anal dysfunction tends to be more severe and prolonged. This exacerbation is attributable to factors such as the lower position of the anastomosis, the surgical resection of a portion or the entirety of the IAS, nerve damage incurred during intraoperative dissection of the ISS, and the involvement of the dentate line's neurosensory area. The intensified clinical manifestation of LARS post-ISR complicates patient management and treatment significantly [4, 17–19]. Consequently, there is a pronounced theoretical and practical imperative to develop an animal model that elucidates the pathophysiological mechanisms underlying postoperative anal dysfunction following ISR. Such a model would be instrumental in devising and evaluating effective strategies to facilitate the restoration of anal sphincter function.
Animal models of ISR have been infrequently documented in the literature. Sato et al [7] observed a significant reduction in anal resting pressure to one-third of its baseline value in pigs after open ISR surgery. Their findings indicated that, one-month post-operation, pigs subjected to ISR and 25% external sphincter resection (ESR) managed to defecate within a singular area, whereas those in the 50% ESR group exhibited defecation across multiple areas alongside severe anal dysfunction, characterized by persistent soiling and discomfort around the anus. Jin et al [8] proposed a method of smooth muscle enrolment and internal sphincter construction (SMESC) to improve continence after ISR for rectal cancer. Their animal model study showed that the SMESC procedure achieved acceptable IAS reconstruction at week 12 without increasing surgical risk. However, these only two investigations, focusing solely on open surgical ISR models, did not replicate the laparoscopic ISR approach utilized in human procedures.
In our study, we leveraged extensive experience from human laparoscopic ISR surgeries to develop the inaugural laparoscopic ISR model in pigs. We defined the criteria for laparoscopic ISR surgery in pigs. According to the consensus of international standardization and optimization group for intersphincteric resection (ISOG-ISR), ISR involves a partial, subtotal or total resection of the IAS via intersphincteric dissection [20]. In our model, we executed a complete resection of the IAS, adhering closely to the prescribed surgical access and extent delineated for ISR procedures.
Pigs are readily available and relatively easy to manage, with their anal canal anatomy similar to humans. This anatomical similarity makes them optimal subjects for the development of surgical models, particularly for ISR. Notably, pigs exhibit a natural inclination to defecate in a specific area of their enclosure, a behavior influenced by the presence of fecal odor. However, those experiencing anal discomfort or damage may display altered defecation patterns, including the tendency to defecate in multiple locations. In response to these observations, we refined the incontinence score table initially proposed by Sato et al. Furthermore, we selected adult Bama miniature pigs for our study due to their suitability for laparoscopic procedures and the potential for in-depth pathophysiological investigations.
Anal function in pigs demonstrated rapid recovery, achieving a plateau approximately 1.5 months post-operatively, in contrast to the 1–2 years required for human patients. The duration of LARS was notably shorter in the porcine model, potentially attributed to the quadrupedal nature of pigs and their inherently stronger perianal musculature. Additionally, the pig's large intestine, characterized by a straight colon and a spiral section, is significantly longer than in humans, promoting the formation of more solid stools.
Our study acknowledges certain limitations. While pig anatomy closely resembles that of humans, notable differences persist. For instance, the anal fissure ligament is less pronounced and the ISS is shorter in pigs, whereas the levator ani muscle (LAM) and EAS exhibit greater strength. Additionally, the structure of the conjoint longitudinal muscle (CLM) and ISS fibers, crucial in human anatomy, are less distinct in pigs. While incontinence scores have provided insights into anal function changes, there is a need to refine these scores for more precise evaluation in the porcine ISR model. Variables such as the average number of defecations per cluster and defecations in lying position have emerged as predictive markers for post-ISR rehabilitation. However, the definition of a defecation cluster and the simulation of nocturnal fecal incontinence by defecations in lying position warrant further clarification and study, as they currently fall outside the scope of traditional incontinence scoring. Further research is needed to address these gaps.