Journal Article Page
European UrologyVolume 63, issue 3, pages e33-e44, March 2013
Parenteral Nutrition Does Not Improve Postoperative Recovery from Radical Cystectomy: Results of a Prospective Randomised Trial
Accepted 28 May 2012, Published online 6 June 2012, pages 475 - 482
After radical cystectomy, patients are in a catabolic state because of postoperative stress response, extensive wound healing, and ileus.
To evaluate whether recovery can be improved with total parenteral nutrition (TPN) in patients following extended pelvic lymph node dissection (ePLND), cystectomy, and urinary diversion (UD).
Design, setting, and participants
We conducted a prospective, randomised, single-centre study of 157 consecutive cystectomy patients.
Seventy-four patients (group A) received TPN during the first 5 postoperative days, with additional oral intake ad libitum. Eighty-three patients (group B) received oral nutrition alone.
Outcome measurements and statistical analysis
The primary outcome was the occurrence of postoperative complications. Secondary outcomes were time to recovery of bowel function, biochemical nutritional (serum albumin, serum prealbumin, serum total protein) and inflammatory (C-reactive protein) parameters, length of hospital stay, and costs attributed to the TPN. The Pearson χ2 test was used for dichotomous variables; the Wilcoxon rank sum test was used for continuous variables.
Results and limitations
Postoperative complications occurred in 51 patients (69%) in group A and in 41 patients (49%) in group B (p = 0.013), a difference resulting from group A having more infectious complications than group B (32% vs 11%; p = 0.001). Serum prealbumin and serum total protein were significantly lower in group B on postoperative day 7 but not on postoperative day 12. Time to gastrointestinal recovery and length of hospital stay did not differ between the two groups. The costs for TPN were €614 per patient. A potential limitation is the use of a glucose-based parenteral nutrition without lipids.
Postoperative TPN is associated with a higher incidence of complications, mainly infections, and higher costs following ePLND, cystectomy, and UD versus oral nutrition alone.
Serious illness, surgery, and postoperative stress response place increased demands on the body's nutritional requirements. These conditions promote a catabolic state that puts the patient at risk of malnutrition. Malnutrition, in turn, leads to higher morbidity, longer hospitalisation, and a higher incidence of hospital-acquired infections  and . Because biochemical signs of malnutrition appear rapidly after major surgery, many intensive care units, especially in Europe, have adopted total parenteral nutrition (TPN) as part of postoperative care following major surgery—including cystectomies —in up to 42% of patients despite adequate gastrointestinal function and even though benefits have only been demonstrated in malnourished patients or in well-nourished patients enduring a postoperative period of semistarvation exceeding 7–10 d , , and . Following radical cystectomy (RC), TPN is also used to prevent hypoproteinemia caused by the extensive wound area. This is especially important, because hypoproteinemia leads to oedema of the bowel wall and thus aggravates the postoperative ileus, a common postoperative complication occurring in up to 25.8% of cystectomy patients . Whether recovery following RC can be improved by postoperative TPN, however, has never been clearly shown , , , and . In the present prospective, randomised trial, we evaluated the clinical impact of TPN versus oral alimentation alone following extended pelvic lymph node dissection (ePLND), cystectomy, and ileal diversion.
2. Patients and methods
2.1. Study population
Between September 2008 and March 2011, 169 consecutive bladder cancer patients scheduled for ePLND, cystectomy, and ileal diversion were assessed for eligibility to enter the study. Exclusion criteria were previous pelvic lymph node dissection (PLND), chronic inflammatory bowel disease, previous radiation therapy, prior bowel surgery, severe hepatic (ascites, portal hypertension, encephalopathy), or cardiac dysfunction (New York Heart Association class greater than III) as well as an inability to give fully informed consent. One hundred fifty-seven patients were included in the study and prospectively randomly allocated by a computer-based program into two groups: group A (n = 74) received TPN, and group B (n = 83) received oral nutrition alone (Fig. 1). Patients with a body mass index (BMI) <18.5, serum albumin <30 g/l, serum prealbumin <0.2 g/l, serum total protein <60 g/l, and/or involuntary weight loss >10% in the preceding 6 mo were defined as malnourished. The study was approved by the local ethics committee. All patients gave their informed consent.
2.2. Patient management
Except for two enemas, each patient received no preoperative bowel preparation. EPLND was performed in every patient, encompassing the obturator fossa and internal, external, and common iliac lymph nodes up to the uretero-iliac junction. The bowel anastomosis was always performed end to end. Perioperatively, a central venous catheter (internal jugular vein) was placed in all patients of both groups. Perioperative antibiotic therapy consisted of an aminoglycoside and metronidazole for 48 h and amoxicillin/clavulanic acid until removal of all stents and catheters. Perioperatively, 3000–4000 ml of parenteral crystalloids were routinely administered. Combined general and epidural anaesthesia was given intraoperatively. Postoperative epidural (T9-T10) analgesia was routinely used, but systemic morphine derivates were avoided. To stimulate postoperative bowel function, subcutaneous injections of 0.5 mg neostigmine methylsulfate up to six times per day were administered to all patients in similar distribution starting on postoperative day 2 and continuing until bowel activity resumed. Antiemetics and other prokinetic drugs were not routinely administered and only given as needed. Low-molecular-weight heparin (Fraxiparine) was started on the evening before surgery and maintained for at least 10 d.
2.3. Nutrition management
None of the patients received any specific preoperative nutrition. TPN consisted of Nutriflex special 70/240 (B. Braun Medical, Melsungen, Germany), a solution with a total energy of 1240 kcal/1000 ml and containing polyamino acids, glucose, and electrolytes. In all group A patients, TPN (1500 ml/d; total 1860 kcal/d; 105 g polyamino acids/d; 360 g glucose/d; 0 g lipids/d) was administered continuously for 5 d starting on postoperative day 1. No intravenous supplementation of vitamins and trace elements was given. An additional 30 IU Actrapid HM (Novo Nordisk, Copenhagen, Denmark) and 1875 IU heparin (Liquemin; Drossapharm, Basel-Stadt, Switzerland) per 24 h were added to the TPN solution. Group B patients were given Ringer's lactate solution (Sintetica–Bioren, Mendrisio, Switzerland; 1500 ml/24 h) and additional potassium substitution (40 mmol/24 h). In both groups, additional glucose 5% (Sintetica–Bioren; 1000 ml/24 h) was administered intravenously for the first 5 postoperative days. Oral alimentation was introduced on postoperative day 1 in both groups with a gastrostomy tube in place, which was initially left on drainage. Oral intake was started with clear fluids on the day of surgery, with fluids started on postoperative day 1. Solid diet was resumed on the return of active bowel sounds and when fluids were well tolerated. The gastrostomy tube was removed after the patient passed stool and tolerated closure of the gastrostomy tube without nausea and vomiting for ≥24 h.
2.4. End points and statistical analysis
The primary end point was the occurrence of postoperative complications within 30 d of surgery according to the Clavien-Dindo classification . Secondary end points were time to recovery of bowel function (nausea, bowel movements, flatulence, passage of stool) as well as nutritional (serum albumin, serum prealbumin, and serum total protein) and inflammatory (C-reactive protein [CRP]) biochemical variables, which were assessed on postoperative days 1, 3, 7, and 12. We also assessed the time to full diet resumption, defined as time until patients tolerated regular intake of solid food of an appropriate amount of calories to cover the basic metabolic rate (1 kcal/h per kg), length of hospital stay, and the additional costs attributed to the infusion solutions. The cost analysis considered the following variables: (1) infusion solutions, (2) infusion set, and (3) laboratory tests for monitoring (glucose, electrolytes). All parameters were assessed by a blinded study nurse.
Statistical analysis was performed by the Institute of Social and Preventive Medicine of the University of Bern, Switzerland, with Stata v.10.0 software (StataCorp, College Station, TX, USA) using the Pearson χ2 test for dichotomous variables and the Wilcoxon rank sum test for continuous variables. Initially, a sample size of 200 patients (100 for each group) was calculated with a one-sided Fisher exact test significance level of 5% (α = 0.05) and a power of 80% (β = 0.2) based on the assumption that the complication rate was 20% in group A receiving TPN and 36.7% in group B receiving oral nutrition alone. However, because infectious complications in group A were more frequent than anticipated, the study was terminated before enrolment targets were met after performing an independent interim statistical analysis.
Preoperative patient characteristics were similar, and the types of urinary diversion (UD) performed were evenly distributed. The median time for surgery and blood loss did not differ between the two groups (Table 1). Postoperative complications occurred in 51 patients (69%) in group A versus 41 patients (49%) in group B (p = 0.013; Fig. 2). There were significantly more infectious complications in group A than in group B (32% vs 11%; p = 0.001). There was no difference in the rate of complications other than infectious complications (p = 0.789; Table 2). The majority of complications (62%) were minor (Clavien-Dindo grade 1 or 2). There were no intraoperative deaths, but early lethal complications (grade 5) occurred in one patient from each group (1%; Fig. 2).
|Characteristic||Group A with parenteral nutrition (n = 74)||Group B with oral nutrition alone (n = 83)|
|Age, yr, median (range)||67 (34−80)||66 (30−86)|
|Gender, no. (%)|
|Male||53 (72)||53 (64)|
|Female||21 (28)||30 (36)|
|BMI, median (range)||25.5 (17.7−35.2)||26.0 (17.2−40.2)|
|Diabetes, no. (%)||6 (8)||8 (10)|
|Malnutrition, no. (%)||11 (15)||23 (28)|
|Kondrup score, no. (%) |
|II||39 (53)||34 (41)|
|III||31 (42)||37 (45)|
|IV||3 (4)||10 (12)|
|V||0 (0)||1 (1)|
|VI||1 (1)||1 (1)|
|ASA score, no. (%)|
|I/II||51 (69)||55 (66)|
|III/IV||23 (31)||28 (34)|
|Neoadjuvant chemotherapy, no. (%)||12 (16)||17 (20)|
|UD, no. (%)|
|Ileal conduit||18 (24)||23 (28)|
|Ileal orthotopic bladder substitute||51 (69)||51 (61)|
|Catheterisable pouch||5 (7)||9 (11)|
|Intraoperative blood loss, ml (range)||800 (250−4000)||850 (300−2000)|
|Time for surgery, min, median (range)||404 (240−465)||400 (305−525)|
BMI = body mass index; ASA = American Society of Anaesthesiologists; UD = urinary diversion.
with parenteral nutrition
(n = 74)
with oral nutrition alone
(n = 83)
|No. *||% of total*||No. *||% of total*|
|Fever of unknown origin||5||7%||2||2%|
|Acute respiratory distress syndrome||2||3%|
|Small bowel obstruction (surgical treatment)||2||3%|
|Temporary renal failure requiring haemodialysis||1||1%|
|Postoperative haematoma (surgical treatment)||1||1%|
|Acute mesenteric ischaemia||1||1%||1||1%|
|Peripheral arterial ischaemia||1||1%|
|Other rare complications||2||3%||3||4%||0.745|
|No postoperative complications||23||31%||42||51%||0.013|
* Patients with multiple complications are counted more than once.
** Ileus is defined as postoperative vomiting associated with abdominal distension requiring cessation of oral intake and/or permanent opening of the gastrostomy tube or the intolerance of oral intake of our patients until postoperative day 5.
UTI = urinary tract infection; MI = myocardial infarction; CHF = congestive heart failure; DVT = deep vein thrombosis.
In all patients, serum albumin, serum prealbumin, and serum total protein dropped significantly after surgery and gradually increased until postoperative day 12 (Fig. 3A–3C). Serum prealbumin and serum total protein were significantly lower in group B than in group A on postoperative day 7 (Fig. 3B–3C). These differences in biochemical parameters had vanished by postoperative day 12. CRP rose significantly after surgery in both groups, showing significantly lower peaks on postoperative day 3 in group A than in group B (p < 0.001; Fig. 3D).
Except for fewer episodes of vomiting on postoperative day 3 in group B, nutrition type had no effect on gastrointestinal function (Fig. 4A–4D). Median time to resumption of full diet (9 d vs 9 d; p = 0.978) as well as the length of hospital stay (16 d vs 15.5 d; p = 0.365) did not differ between the two groups. The costs attributed to TPN were €614 per patient.
A post hoc analysis performed on the subgroup of patients classified preoperatively as malnourished (n = 34) showed no significant difference in overall (82% vs 52%; p = 0.096) or infectious (18% vs 13%; p = 0.692) complication rates between group A malnourished patients (n = 11) versus group B malnourished patients (n = 23). Except for a significantly lower serum prealbumin level on postoperative day 7 in group B (median 0.19 g/l vs 0.14 g/l; p = 0.011), no differences in nutritional or inflammatory biochemical variables were observed between the two malnourished subgroups.
RC combined with ePLND and UD is an extensive surgical procedure causing a high rate of postoperative complications . The complications are related to many factors, including surgical trauma, intestinal oedema, and blood loss. The present randomised study was initiated to determine whether TPN can reduce the incidence of postoperative complications. Surprisingly, our findings show that postoperative TPN was associated with an increased rate of infectious complications as well as with higher costs. This finding is in line with the findings of a large meta-analysis on parenteral nutrition  and of another meta-analysis analysing the outcome of early enteral versus parenteral nutrition . Possible reasons for the adverse effect of TPN are first, that parenteral nutrition impairs the immune system by causing dysfunction of B and T lymphocytes, macrophages, and neutrophils . Second, TPN raises blood glucose levels, making insulin treatment necessary, which in turn appears to have a negative impact on the immune system and increases susceptibility to infection  and . Third, TPN leads to intestinal mucosal atrophy with consequent increased intestinal permeability favouring bacterial translocation; in contrast, enteral nutrition prevents adverse structural and functional alterations of the gut barrier, improves intestinal blood flow, and increases the systemic and local immune response , , and . Finally, TPN increases the risk of catheter-related bloodstream infections  and .
In contrast to the assumption of Maffezzini et al. that early postoperative provision of artificial nutrients, whether in the form of TPN or enteral nutrition, has beneficial effects , our data show that TPN is associated with a higher rate of infectious complications. Some patients, however, experience prolonged postoperative ileus and do not tolerate oral intake in the first postoperative days. In these critically ill patients, parenteral nutrition should be considered if (semi)starvation lasts for >7–10 d  and  so as to prevent the serious adverse effects of long-term protein-energy malnutrition.
Elevated CRP is the most important indicator of acute-phase reaction. It is generally acknowledged that early postoperative CRP plasma concentrations are an indicator of the degree of trauma inflicted upon the organism by surgery, with a peak on postoperative day 3 . This finding is in line with our findings. The significantly lower CRP values on postoperative day 3 in our patients receiving TPN contrast with the higher rate of infection in this group. Nevertheless, >90% of the infectious complications occurred later than postoperative day 3. A possible explanation is that TPN may have contributed—at least to some extent—to the lower CRP levels by negatively influencing the function of T lymphocytes and macrophages, both of which secrete interleukin-6, which in turn stimulates CRP production. However, lower CRP values in patients receiving postoperative TPN versus patients receiving postoperative enteral nutrition alone was not found in other studies  and .
Serum prealbumin and serum total protein were restored earlier in group A patients. However, this result had no impact on clinical outcome. This finding is in contrast to the results of Maffezzini et al. , who did not find any effect of early postoperative parenteral nutrition on postoperative protein depletion. However, they measured serum albumin and serum total protein only on postoperative days 3 and 5, whereas we could show that postoperative normalisation of the serum proteins takes ≥7 d. This delay is most probably the result of transcapillary escape of serum proteins into the interstitial fluid during the first postoperative days, a phenomenon that largely depends on the surgical trauma and its consequent systemic inflammatory response syndrome .
Like Maffezzini et al. , we found no significant difference in time to recovery of bowel function in our patients. The 13% incidence of postoperative ileus—defined as postoperative vomiting associated with abdominal distension requiring cessation of oral intake and/or permanent opening of the gastrostomy tube or the intolerance of oral intake of our patients until postoperative day 5—is in line with the findings of others  and . Although delayed postoperative return of bowel function is acknowledged to be the most frequently encountered complication after RC, high variability exists in the incidence of postoperative ileus, most probably because of the different definitions used for this condition , , and . We therefore analysed not only the incidence of postoperative ileus but also other objective, measurable parameters such as bowel movements, flatulence, and passage of stool, although these parameters have their own observer and time-dependent weaknesses.
Our overall 59% complication rate also agrees with the results of another major centre using a standardised prospective reporting methodology . The majority of complications (62%), however, were minor (grade 1 or 2; Fig. 2). At the time the present prospective study was performed, our anaesthetists routinely administered high volumes of parenteral crystalloids perioperatively. Doing so is known to significantly increase postoperative complications as well as postoperative body weight resulting from, for example, intestinal oedema  and might have negatively influenced perioperative blood loss. The extent to which this high-volume perioperative fluid management may have negatively influenced our results remains unknown; we recently abandoned it in favour of increased use of vasoactive agents to compensate for the anaesthesia/analgesia-induced vasodilation.
A potential limitation is that we only used a standard TPN solution containing polyamino acids, glucose, and electrolytes. Other parenteral nutritional supplementations are available (eg, with lipids), although several reports have shown that lipids adversely affect immune status, complications, and clinical outcome . In addition, more inflammatory and immunologic markers could have been used. It should be noted, however, that the main focus of the study was the patients’ clinical outcome. Another limitation is that the study had to be stopped early because of the potential harm of TPN, which may have influenced results to some extent.
There is no evidence that withholding parenteral nutrition for at least 7 d is harmful in patients who are not severely malnourished . Still, precise diagnosis of malnutrition is difficult, because there is no standardised and widely accepted definition. This major methodological shortcoming contributes to the heterogeneity of findings among studies , , , and . Using our definition for malnutrition, the prevalence of preoperative malnutrition in our patients was 22%. In contrast to the findings of some authors , , and  but in line with Bozzetti et al.  and Mohler et al. , our post hoc subgroup analysis could not demonstrate any clinical benefit of TPN for malnourished patients with regard to preventing postoperative complications. Still, our subgroup analysis is underpowered and does not allow for any definitive conclusions.
The findings of the present prospective, randomised study show that postoperative TPN following ePLND, cystectomy, and ileal diversion has considerable disadvantages in terms of a higher rate of complications—mainly infectious—when compared to postoperative oral alimentation alone. We therefore cannot recommend TPN as part of standard postoperative management following ePLND, cystectomy, and ileal diversion.
Author contributions: Urs E. Studer had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Studer, Burkhard, Huwyler, Thalmann, Roth.
Acquisition of data: Roth, Huwyler, Zehnder, Birkhaeuser.
Analysis and interpretation of data: Roth, Studer.
Drafting of the manuscript: Roth.
Critical revision of the manuscript for important intellectual content: Studer, Birkhaeuser, Zehnder.
Statistical analysis: Roth, Studer (external analysis).
Obtaining funding: None.
Administrative, technical, or material support: None.
Supervision: Studer, Burkhard, Thalmann.
Other (specify): None.
Financial disclosures: Urs E. Studer certifies that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None.
Funding/Support and role of the sponsor: None.
Trial registration: ClinicalTrials.gov; ISRCTN79535150.
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Department of Urology, University of Bern, Bern, Switzerland
© 2012 European Association of Urology, Published by Elsevier B.V.
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