Surgical and medical co-management optimizes surgical outcomes in older patients with chronic diseases undergoing robot-assisted laparoscopic radical prostatectomy

Abstract Introduction While robotic-assisted laparoscopic radical prostatectomy (RRP) is a standard mode for localized prostate cancer (PC), the risk of complications in older patients with chronic diseases and complex medical conditions can be a deterrent to surgery. Surgical and medical co-management (SMC) is a new strategy to improve patients’ healthcare outcomes in surgical settings. Methods We reviewed the clinical data of older patients with chronic diseases who were cared for with SMC undergoing RRP in our hospital in the past 3 years and compared them with the clinical data from the general urology ward. Preoperative conditions and related indicators of recovery, and incidence of postoperative complications with the Clavien Grade System were compared between these two groups. Results The indicators of recovery were significantly better, and the incidence rates of complications were significantly reduced in the SMC group at grades I–IV (p < 0.05), as compared to the general urology ward group. Conclusions The provision of care by SMC for older patients focused on early identification, comorbidity management, preoperative optimization, and collaborative management would significantly improve surgical outcomes. The SMC strategy is worthy of further clinical promotion in RRP treatment in older men with chronic diseases and complex medical conditions.


Introduction
Prostate cancer (PC) has become the second most common cancer among men in the world and tends to occur in older patients [1][2][3].Robot-assisted laparoscopic radical prostatectomy (RRP) is the standard mode of treatment for localized PC [4].With decreased invasiveness, RRP surgery is recommended for geriatric patients.Studies have shown that older adults with chronic diseases and complex medical conditions undergoing RRP experience higher rates of postoperative complications than younger patients [5,6].Increased rates of postoperative complications among older adults in RRP are likely attributable to an increased prevalence of chronic comorbidities or commonly recognized age-related changes in health, as well as the steep Trendelenburg position and high intraoperative ventilatory pressure of pneumoperitoneum [7].When considering surgery therapy, perioperative risks are discussed and may be a deterrent to pursuing surgical treatment in older patients with localized PC.Randomized clinical trials provide evidence that radical prostatectomy improves overall survival or delays the development of metastatic disease compared with observation (watchful waiting).A mean of 2.9 extra years of life was gained with radical prostatectomy [8].Indeed, surgical therapy may be appropriate for older patients if their disease risk can be early identified and optimized [9].Considering these factors, it is certainly rational that internists should be included in a collaborative model of surgical and medical co-management (SMC) so that they could coordinate within the multidisciplinary team.
SMC is a collaborative model between internists and surgeons for the care of high-risk surgical patients.In this type of collaborative model, the internist is asked to assume the management of specific aspects of the patient's care.The internists choose which test to perform and which treatment to implement [10].SMC model is a testified strategy to improve health care outcomes for high-risk surgery patients in abdominal surgery [11,12] and hip surgery [13].However, its application in patients undergoing urological surgery has rarely been studied.To date, there is no report to compare the efficacy and safety of SMC in conventional care for patients undergoing RRP.Whether the SMC pathway can benefit older patients with chronic diseases and complex medical conditions undergoing RRP remains inconclusive.
We hypothesized that the provision of care by SMC for high-risk older PC patients would significantly impact operative complications and health outcomes.Therefore, we sought to compare the outcomes of high-risk men undergoing SMC mode and traditional urological surgery management mode at the Chinese PLA General Hospital (PLAGH), to assess the efficacy of SMC mode in this population of men.

Ethics statement
The PLAGH ethics committee institutional approved this study and authorized waived informed consent since the study was observational.

Participants
Between January 2019 and January 2022, the SMC team treated 92 older adults undergoing RRP at the PLAGH.Patients were assessed within 30 days before surgery and co-treated by internists and urological surgeons throughout their hospitalization.This SMC cohort was compared with a case-matched control group of patients who underwent the traditional model.Selection criteria were used to give a framework for identifying older adults considered to be at higher risk.Patients over 65 years were considered eligible when any one of the following conditions was present: prior diagnosis of multimorbidity (presence of 2 or more chronic medical conditions), polypharmacy [12] (more than 5 prescription medications).

The SMC model group
The participants were admitted into a comprehensive surgery ward under the co-management care of urological surgeons and internists.The relationship between the internist and the surgeon is collaborative, and both are intimately involved in medical decisionmaking.Usually, the internists have the latitude to write orders, participated in rounds daily, and choose which test to perform and which treatment to implement for risk-reducing strategies.To facilitate the implementation of recommendations made before surgery, the inpatient internists team collaborated with the surgical teams, assisting with the management of medications, chronic medical conditions, pain, and recognition and treatment of common postoperative complications.According to the characteristics of RRP  1.

Control group
The control group of participants comes from the general urology surgery ward who were older than 65 years and underwent the same surgical procedures, performed by the same surgical group, between January 2019 and January 2022.In the control group, the participants received the specialist cure from urological surgeons only, the internist evaluates chronic medical conditions and operation risk by consultation only at the request of the surgeon.

Study variables and data collection
Data from SMC patients were collected during a standardized preoperative assessment using prescribed intake forms for each discipline.Because the control group had no preoperative geriatrics assessment, baseline data for this analysis were collected from administrative data and medical record review using medical record numbers for both SMC and control groups: Age, clinical stages, current smoking status, history of alcohol intake, body mass index (BMI), metabolic equivalent (MET), medications, chronic comorbidities, the score of American Society of Anesthesiologists (ASA) and laboratory values.Perioperative information including total anesthesia time, skin-to-skin operation time, pneumoperitoneum time, estimated blood loss, total vein fluid, and incidence of perioperative hypotension (was defined as an average arterial pressure lower than 65 mmHg and lasted for more than 10 min [14]).
Postoperative conditions including early recovery parameters were compared between these two groups: pain score, time to the beginning of ambulation and diet, time to the opening of the bowel (passage of flatus/stools), and time to removing of nasogastric tube and intra-abdominal drain catheter, and the difference of hemoglobin and serum albumin within 3 days before and after the operation, and duration of catheterization.
Postoperative complications were divided into grades I, II, III, and IV according to Clavien Classification System [15].Grade I: the complications had mild impacts on patients' recovery, and these antipyretics, analgesics, antiemetics, diuretics, and physical therapy were allowed to apply.Grade II: on the basis of grade I, other kinds of drugs, blood infusion, or total intravenous nutrition were required.
Grade III: surgery, endoscope, or radiotherapy were required.Grade IV: the former one's complications having life threats to the patients, who showed single organ failure, and the latter one manifested as multiple organ failure.The incidence of perioperative complications in patients was observed and recorded.

Statistical analysis
All statistical analysis tests were carried out with SPSS 22.0 software (SAS Institute, Cary, NC, USA).Measurement data were represented as mean ± SD, and comparisons between groups were performed by independent sample t-test.Categoric distributions are reported as counts.A two-tailed p-value of <0.05 was considered statistically significant.

Patient and surgery characteristics
The patients who utilized the SMC model had an older mean age and greater burden of medical illness: age, mobility, and ASA scores were worse (Table 2).There was no statistically significant difference in BMI, tumor stage, current smoke, alcohol intake, polypharmacy, concomitant medical diseases, and most laboratory values between the SMC group and the traditional surgery group.
There was no statistically significant difference in anesthesia time, skin-to-skin operation time, pneumoperitoneum time, or estimated blood loss between the two groups.Total intraoperative fluid volume was higher in the traditional group as compared to the SMC group and was statistically significant.The presence of hypotension is more frequent in the traditional surgery group as compared to the SMC group.The operative data are shown in Table 3.

Postoperative conditions
The patients who utilized the SMC model experienced faster recovery.The patients who underwent SMC experienced a lower level of pain score and were more willing to ambulate earlier as compared to the traditional group.The time of removing the gastric tube and recovery oral diet was early in the SMC group and was statistically significant.The laboratory deference in hemoglobin and serum albumin were significantly lower in the SMC group as compared to the traditional surgery group.The time of removing the intra-abdominal drain catheter was also early in the SMC group.There was no statistically significant difference in days of catheterization.The details of postoperative data are shown in Table 4.

Comparison of postoperative complications by Clavien Classification System
Overall, postoperative complications were classified by the Clavien Classification System in Table 5.There were fewer complications of grades I-IV in the SMC group than in the traditional group significant, respectively [(16.3% vs. 29.3%,14.1% vs. 28.3%,1.1% vs. 7.3%, 1.1% vs. 8.7%), all p < 0.05)].The differences in grade II complications were the most significant (p ¼ 0.019).The pulmonary, cardiovascular, neurological, gastrointestinal, urinary, and vascular (only grades II) system complications at grades I-II in the  SMC group were significantly lower than that in the control group, respectively (all p < 0.05).The pulmonary, neurological, gastrointestinal, urinary, and vascular system complications were rare at grades III and the neurological, gastrointestinal, and urinary system complications were rare at grades IV.There was no statistically significant difference in surgical site complication rate at grades I-IV between these two groups.

Discussion
In our study, the provision of care by the SMC model for high-risk older patients in prostatectomy has focused on early risk identification and medical conditions optimization and provided sequential treatment in three stages: preoperative, operative, and postoperative stages, attributable to the good collaboration between internists and surgeons.We assessed whether the SMC model is a safe and effective procedure for reducing postoperative complications in urological complicated operations.To our knowledge, this is the first study of the SMC model used in prostatectomy patients that have shown sustained complications reduction, together with improved recovery ability.
The RRP is one of the most complicated and technically demanding operations in the urological ward which has increased rapidly in older high-risk patients.It is necessary that reduce perioperative complications and accelerate of patient's recovery.SMC management of surgical patients refers to patient care in which an internal medicine physician assesses acute issues daily, addresses medical comorbidities, communicates with surgeons, and facilitates patient care transition from the acute care hospital setting.Moreover, due to the  existence of written orders, the recommendations of internists have a better chance to be followed in time.In our study, the internist and the surgeon are collaborative, and both are intimately involved in medical decision-making.This model can avoid problems concerning the transmission of information, the urgency of consultation, unjustified repetitions, and delays in the request.Co-management by internists has demonstrated value for high-risk surgery in orthopedic, vascular, and colorectal surgery, but has not been reported in urological surgery [12,[16][17][18].Our study, for the first time, demonstrated that the RRP patients who utilized the SMC model experienced faster recovery and significantly lower rates of complications, regardless of older mean age and greater burden of medical illness.
Early preoperative risk identification and medical conditions optimization for surgery risk reduction are important aspects of clinical practice in perioperative medicine.Several approaches to perioperative risk stratification have been proposed with risk scores and additional testing including cardiopulmonary exercise testing [19,20].High-risk patients could benefit from the optimization of their physical and mental status to minimize the risk of adverse events [21].In our study, internists identify comorbidity disease conditions by providing risk stratification and performing interventions for the optimization of their physical and mental status.The SMC process follows preoperative assessment and management guidelines, which recommend specific steps for improving care in several domains, including cognition, nutrition, mobility, medication management, and caregiving.With this approach, patients' medical comorbidities would be optimized preoperatively to prevent organ dysfunction by surgery injury.
Intraoperative hypotension in patients undergoing non-cardiac surgery with general anesthesia can result in tissue hypoperfusion and subsequent organ damage [14,22].In our study, the SMC team pays attention to fluid management and plays important role in fasting for surgery.The team guides patients' oral administration of at least 1000 mL of carbohydratecontaining liquid before the surgery.Maintaining cardiac preload throughout the perioperative period is a generally accepted target [23,24].The internists can identify or even predict before hypotension becomes clinically significant and apply pre-emptive treatment strategies to reduce the incidence or duration of hypotensive episodes.We observed that the incidence of perioperative hypotension was significantly reduced in the SMC group, as compared with the control surgery group.Further, the postoperative complications were reduced.
The major adverse events leading to death commonly occur in the first 24 h after surgery [25].Monitoring systems in the operating room or intensive care units (ICU) enable numerical and waveform blood pressure data to be processed and displayed continuously in real-time [26].Under the SMC mode, patients were admitted to the ICU for 24 h postoperatively and follow-up on the ward by co-management teams.The high-risk patients benefited from improved peri-operative surveillance and complex care management with regular risk assessments.The indicators of early postoperative recovery were significantly improved as compared with those of the control surgery group.The SMC group had a significantly shorter time to the first defecation, a shorter time to the first anal exhaust, and a lower incidence of nausea as compared to the conventional care group.The pain score and the rate of arrhythmia, delirium, and acid-base imbalance water-electrolyte disorder were also reduced.
The older age of patients diagnosed with PC increases the prevalence of various comorbidities, including ischemic heart diseases, diabetes mellitus, and hypertension, making these patients susceptible to adverse hemodynamic changes during surgery adversely [27].The development of at least 1 postoperative cardiovascular or pulmonary complication, even those presumed mild, was associated with significantly increased early postoperative mortality [28].Plasma albumin and hemoglobin levels are closely related to postoperative complications [29,30].This study found that there was no significant difference between the two groups of operative blood loss, but the differences in hemoglobin and albumin before and after the operation were significantly less in the SMC group.There are two potential underlying reasons: the infusion quantity in the co-management group was significantly reduced to avoid the influence of blood dilution on hemoglobin and albumin levels; effective nutritional support therapy could reduce the consumption of hemoglobin and albumin.To reduce these complications, the SMC team identified potentially modifiable factors for future targeted interventions, including colloid administration, low preoperative oxygenation, blood loss, anesthesia duration, intraabdominal pressure, lower temperature, and intraoperative median tidal volume.Efforts to reduce these factors may contribute to improved perioperative outcomes and shortened hospital stays.The SMC team used effective prevention strategies and had significantly lower rates of cardiopulmonary complications.
Our conclusion is limited by the nature of a singlecentered study with a limited sample size.Large-scale, multi-center, and well-designed studies are required to verify and extend our conclusion.Such studies are also necessary to identify additional metrics affected by the program.Lastly, our results may in part be attributable to certain characteristics of the Chinese healthcare stem and may not be generalized in countries with different health systems.

Conclusion
SMC protocols employ multimodal and multidisciplinary efforts to optimize patient care in the preoperative, operative, and postoperative settings.The provision of care by SMC for older with chronic diseases and complex medical conditions focused on early risk identification, comorbidity management, preoperative optimization, and collaborative management to significantly improve perioperative outcomes.SMC represents a shift in the traditional model of health care for surgical patients, from a reactive and ondemand model to a pro-active and continuity model, from a late and complication treatment-based model to an early and preventive one.These support the shift away from the single-disease model in healthcare to a more holistic construct, emphasizing considering multimorbidity composition in clinical decision-making, and are worthy of further clinical promotion.
Early respiratory muscle training (after pre-operative training) Careful reintroduction of patient's chronic medication Medicine for prostate cancer surgery, interventions that are performed for optimization are shown in Table

Table 2 .
Patient characteristics at baseline.
a MET: metabolic equivalent; b ASA classification: I ¼ normal healthy patient; II ¼ mild systemic disease; III ¼ severe systemic disease.

Table 3 .
Operative parameters.Hypotension was defined as an average arterial pressure lower than 65 mmHg and lasted for more than 10 min. a

Table 5 .
Comparison of postoperative complications by Clavien Classification System.