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Anesth Analg 2000;91:1176-1181
© 2000 International Anesthesia Research Society

ECONOMICS AND HEALTH SYSTEMS RESEARCH

Longer-Term Diabetic Patients Have a More Frequent Incidence of Nosocomial Infections After Elective Gastrectomy

Soichiro Yamashita, MD*, Hiroshi Yamaguchi, MD*, Misa Sakaguchi, MD*, Tsuyoshi Satsumae, MD*, Sumii Yamamoto, MD*, and Fumiaki Shinya, MD{dagger}

Departments of *Anesthesia and Critical Care Medicine and {dagger}Surgery, Iwaki Kyoritsu General Hospital, Uchigo, Iwaki, Fukushima, Japan

Address correspondence and reprint requests to Hiroshi Yamaguchi, MD, Department of Anesthesia and Critical Care Medicine, Iwaki Kyoritsu General Hospital, Uchigo, Iwaki, Fukushima, 973-8555, Japan. Address e-mail to hyanchi{at}aol.com


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Diabetes mellitus (DM) is one of the risk factors for the development of postoperative nosocomial infections in surgical patients. We conducted this retrospective study to elucidate the perioperative risk factors for postoperative nosocomial infections in diabetic patients undergoing elective gastrectomy. Chart review was performed on diabetic and nondiabetic patients undergoing elective gastrectomy for gastric malignancy from January 1992 through April 1999. Fourteen of the 83 diabetic patients, and 23 of the 284 nondiabetic patients developed postoperative nosocomial infections. Statistical comparisons of multiple variables were made between patients with and without postoperative nosocomial infections. In diabetic patients, univariate analysis showed that longer-term DM (especially longer than 10 yr) was associated with a significantly increased risk for postoperative nosocomial infections. Multiple logistic regression analysis showed that DM lasting longer than 10 yr was an independent risk factor for postoperative nosocomial infections (odds ratio, 6.8; 95% confidence interval, 1.7 to 27.1). In nondiabetic patients, similar analysis showed that age was an independent risk factor for postoperative nosocomial infections. We conclude that patients with longer-term DM had a significantly greater incidence of postoperative nosocomial infections after elective gastrectomy.

Implications: Postoperative nosocomial infection is one of the major problems in diabetic patients. This study demonstrated that postoperative nosocomial infections were more common in patients undergoing elective gastrectomy if they had diabetes mellitus longer than 10 yr.


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Although antibacterial drugs and aseptic surgical management modalities exist, postoperative nosocomial infections continue to be common complications in surgical patients and result in increased mortality, morbidity, and hospital costs. Characteristics that are associated with an increased risk for postoperative nosocomial infections include extremes of age, cigarette smoking, poor nutritional status, obesity, duration of surgery, and surgical technique (1–3).

Diabetes mellitus (DM) is one of the major risk factors in surgical patients contributing to the development of postoperative nosocomial infections. The critical role played by polymorphonuclear neutrophils (PMNs) in host defense mechanism against infection has encouraged the studies of various aspects of neutrophil function in diabetic patients (4–8). Poor control of blood glucose level impairs PMNs’ functions, including adherence, chemotaxis, phagocytosis, and bacterial killing activities. Diabetic patients may also be prone to endogenous infections. Colonization by abnormal flora, in particular aerobic Gram-negative bacilli, is substantially more common in diabetic patients than in control subjects (9). Carriage of abnormal flora in the digestive tract is a risk factor for subsequent nosocomial infections in different populations (10,11).

However, it is controversial whether demographic data and/or perioperative laboratory findings play a role in the development of postoperative nosocomial infections in diabetic patients. We conducted this retrospective study to elucidate the perioperative risk factors contributing to the development of postoperative nosocomial infections in diabetic patients undergoing elective gastrectomy.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
Population
This study protocol was approved by our local ethics committee. We performed a retrospective chart review on surgical patients undergoing elective gastrectomy for gastric malignancy performed in our hospital from January 1992 through April 1999. Excluded from this study were patients with clinical evidence of preoperative infections (n = 3), immunocompromised patients (n = 4), patients who underwent additional resection of pancreatic tail (n = 85) or colon segment (n = 14), patients who underwent laparoscopic or partial gastrectomy (n = 5), patients who received repeated surgery not mainly the result of infection postoperatively (n = 9), and patients who died not as a result of infection postoperatively (n = 7). Three hundred sixty-seven patients (83 diabetic and 284 nondiabetic patients) undergoing elective gastrectomy for gastric malignancy were enrolled in this study.

Definition of Postoperative Nosocomial Infections
The development of postoperative nosocomial infection was defined as present when the patients met the criteria during the first postoperative 30-day period (12–14). Surgical wound infection was diagnosed when there was purulent discharge from the incisional wound, excluding minimal inflammation and discharge confined to the points of suture penetration. Intraabdominal infection was diagnosed when there was purulent discharge from a drain or confirmation by radiograph, computed tomography, or ultrasound examinations. Gastrointestinal tract infection was diagnosed when enteric pathogens were isolated from stool culture with acute onset of diarrhea. Pulmonary infection was diagnosed when predominant organisms were isolated from purulent sputum culture and a new or changing infiltrative shadow on chest radiograph with evidence of systemic infection (body temperature above 38.0°C, and leukocytosis >10,000 or <5,000). Urinary tract infection was diagnosed when more than 105 organisms per milliliter of urine were isolated with evidence of systemic infection. Catheter-related infection was diagnosed when organisms were isolated from catheter tips’ culture in the setting of suspected infection (systemic symptoms or localized purulence). Bloodstream infection was diagnosed when organisms were isolated from blood cultures from any site with the exception of Staphylococcus epidermidis or other coagulase-negative staphylococci.

Variables of this Study
The data were collected through the patients’ chart review. The following patient-related factors were recorded: sex, age, body mass index (weight in kilograms divided by height in meters squared), ASA physical status, DM, hypertension, coronary artery disease, cardiac insufficiency, cardiac arrhythmia, pulmonary disease, renal insufficiency, liver insufficiency, central nervous system disease, and preoperative laboratory findings (fasting blood glucose level, serum total protein level, serum triglyceride level, and serum total cholesterol level).

The following surgery-related factors were recorded: pathology of gastric malignancy (cancer, lymphoma, or sarcoma), type of surgical procedure (distal gastrectomy, proximal gastrectomy, or total gastrectomy), extension of the resections onto other organs, reconstructions, surgeons, duration of surgery, and antibiotic prophylaxis given.

In diabetic patients, in addition to the above, the following DM-related factors were recorded: insulin dependent (type I) or noninsulin dependent (type II) DM, DM duration since its diagnosis, main antidiabetic therapy (none, diet only, oral hypoglycemic drugs, or regular insulin use), serum hemoglobin A1c level, diabetic nephropathy, diabetic neuropathy, diabetic retinopathy, and postoperative blood glucose control (daily mean blood glucose levels on the first through the fifth postoperative day). Daily mean blood glucose levels were calculated by averaging the values determined by using finger stick measurement (TIDETM, Leverkusen, Germany) three times a day.

Diabetic patients (n = 83) of the 367 patients undergoing elective gastrectomy were divided into two groups: those with postoperative nosocomial infections (Infection Group, n = 14) and those without postoperative nosocomial infections (No Infection Group, n = 69). Statistical comparisons of multiple variables were made between the Infection and the No Infection Groups to find the perioperative DM-related factors contributing to the development of postoperative nosocomial infections in diabetic patients undergoing elective gastrectomy.

Nondiabetic patients (n = 284) of the 367 patients undergoing elective gastrectomy were divided into two groups: those with postoperative nosocomial infections (Infection Group, n = 23) and those without postoperative nosocomial infections (No Infection Group, n = 261). Statistical comparisons of multiple variables were made between the Infection and the No Infection Groups to find the perioperative factors contributing to the development of postoperative nosocomial infections in nondiabetic patients undergoing elective gastrectomy.

Statistical computer application, Stat-View, version 0.5 (SAS Institute, Cary, NC), was used for statistical analysis. Univariate analysis was performed by using the two-tailed Student’s t-tests for parametric variables, the Mann-Whitney ranked sum test for nonparametric variables, and the {chi}2 test (or Fisher’s exact test, where appropriate) for categorical variables. P < 0.05 was considered statistically significant. To control for potential confounding variables, the variables with a P value of <0.2 in the univariate analysis were entered into a multiple logistic regression analysis.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Fourteen patients (16.9%) of the 83 diabetic patients undergoing elective gastrectomy developed postoperative nosocomial infections. Five had surgical wound infections, two had intraabdominal infections, one had liver abscess, five had pneumonia, one had catheter-related infection, and one had bloodstream infection. Two of these patients had sepsis and eventually died as a result of multiple organ failure. Twenty-three patients (8.1%) of the 284 nondiabetic patients undergoing elective gastrectomy developed postoperative nosocomial infections. Eight had from surgical wound infections, seven had intraabdominal infections, one had cholecystitis, three had bacterial colitis, two had pneumonia, and five had catheter-related infections. One of these patients had sepsis and eventually died as a result of acute renal failure. The incidence of postoperative nosocomial infection in diabetic patients was significantly greater than in nondiabetic patients (P = 0.0196).

Diabetic patients who developed postoperative nosocomial infections had significantly longer hospital stays after surgery than those who did not (62.4.0 ± 19.0 vs 35.6 ± 12.0 days, P < 0.0001). Nondiabetic patients who developed postoperative nosocomial infections also had significantly longer hospital stays after surgery than those who did not (55.1 ± 29.5 vs 35.2 ± 13.1 days, P < 0.0001).

A univariate analysis of potential risk factors for the development of postoperative nosocomial infections in diabetic and nondiabetic patients undergoing gastrectomy was performed (Table 1). Significant risk factors for the development of postoperative nosocomial infections in diabetic patients was the DM duration (P = 0.0435). Figure 1 shows the relationship between the incidence of postoperative nosocomial infections and the DM duration. Patients with DM longer than 10 yr are significantly more prone to have postoperative nosocomial infections compared with those with DM less than 10 yr (P = 0.0039). The postoperative blood glucose levels showed no significant difference between diabetic patients who developed postoperative nosocomial infections and those who did not (Figure 2). The variables with a P value of <0.2 in the univariate analysis were entered into a multiple logistic regression analysis. DM lasting longer than 10 yr was independently associated with a significantly increased risk for the development of postoperative nosocomial infections in diabetic patients undergoing gastrectomy (odds ratio, 6.8; 95% confidence interval, 1.7 to 27.1). The significant risk factor for the development of postoperative nosocomial infections in nondiabetic patients was age (P = 0.0254). Age was independently associated with a significantly increased risk for the development of postoperative nosocomial infections in nondiabetic patients undergoing gastrectomy (odds ratio, 1.052; confidence interval, 1.003 to 1.104).


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  		Table 1. Comparisons of Variables in Diabetic and Nondiabetic Patients (Univariate Analysis)
 


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  		Figure 1. The relationship between the incidence of postoperative nosocomial infections and the diabetes mellitus (DM) duration in diabetic patients. Note that patients with DM longer than 10 yr had a significantly greater incidence of postoperative nosocomial infections compared with those with DM shorter than 10 yr (P < 0.005).

 


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  		Figure 2. Daily mean blood glucose levels on the first through the fifth postoperative day (POD) after surgery with or without postoperative nosocomial infections in diabetic patients. The postoperative blood glucose levels showed no significant difference between the Infection and the No Infection Groups.

 
The organisms grown by site are shown in Table 2. Forty-four isolates were obtained from the 37 patients who developed postoperative nosocomial infections. Aerobic Gram-negative bacilli were obtained from 18 patients (48.6%) and methicillin-resistant S. aureus from 12 patients (32.4%). Most patients were given prophylactic antibiotics (2 g per day) (Table 1) IV from 30–60 min before skin incision to the fourth postoperative day. The type of prophylactic antibiotics were not associated with the cultured organisms of postoperative nosocomial infections. Patients who developed postoperative nosocomial infections were treated by using IV administration of another antibiotic sensitive to the cultured organisms, and surgical drainage when necessary.


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  		Table 2. The Microorganisms Grown by Site
 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
The results of this study indicate that diabetic patients undergoing gastrectomy have a more significantly increased risk for the development of postoperative nosocomial infections than nondiabetic patients. Especially, the longer-term DM (longer than 10 years) patients had a particularly significant correlation with the development of postoperative nosocomial infections.

The findings of this study may support the pathophysiologic changes in patients with longer-term DM. First, leukocyte function may be impaired in patients with longer-term DM. In the study on myoinositol metabolism in leukocytes, it is suggested that abnormal myoinositol transport is associated with prolonged hyperglycemia (15). Sato et al. (6) suggested that myeloperoxidase activity in leukocytes is reduced by the continuation of hyperglycemia. Second, vascular complications may occur in patients with longer-term DM. Arteriosclerosis and microangiopathy may impair peripheral circulation. Tissue hypoxia may delay wound healing. Furthermore, impaired peripheral circulation may decrease antibiotic absorption (8). Third, polyneuropathy may occur in patients with longer-term DM. Autonomic involvement of the bladder may lead to urine retention, which predisposes to bacteriuria (16). Autonomic involvement of bowel function may lead to gastric overgrowth that is an independent risk factor for wound infections after gastrectomy (17) because slow intestinal transit can allow bacteria to proliferate in the lumen (18). Impairment of oropharyngeal function may lead to pulmonary aspiration, which predisposes to pneumonia (19), and can be an increased risk factor for Gram-negative bacillary pneumonia associated with an increased prevalence of pharyngeal abnormal flora in diabetic patients (9,20).

In nondiabetic patients, age was an independent risk factor for the development of postoperative nosocomial infections. In diabetic patients, mean patient age in the Infection Group was higher than that in the No Infection Group, but without a significant difference. A multiple logistic regression analysis showed that DM lasting longer than 10 years was an independent risk factor for the development of postoperative nosocomial infections. However, the DM duration can be closely related to age. So, we may have to consider the influence of pathophysiologic changes caused not only by DM, but also by aging, on the development of postoperative nosocomial infections.

The results of this study showed no correlation between mean postoperative blood glucose levels and the development of postoperative nosocomial infections. In one study, an increased risk for postoperative nosocomial infections was observed in diabetic patients with poor blood glucose control. Pomposelli et al. (21) showed that the highest blood glucose level more than 220 mg/dL on the first postoperative day was associated with an increased risk for postoperative infections in diabetic patients, but their study was performed by using diabetic patients undergoing various kinds of surgery including cardiac, abdominal, and orthopedic. The kind of surgery should be uniform to find the contributing risk factors. Zerr et al. (22) demonstrated that a protocol with the goal of maintaining postoperative blood glucose level less than 200 mg/dL through the use of an insulin infusion led to fewer deep sternal wound infections in diabetic patients undergoing cardiac surgery. However, cardiac surgical patients cannot be compared equally with gastric surgical patients who are exposed to risk factors (bacterial contamination, anastomotic dehiscence, or aspiration) for the development of postoperative nosocomial infections.

A German prospective trial showed a significant reduction in infectious morbidity by using selective digestive decontamination (SDD) by oral application of nonresorbable bactericidal antibiotics as a valid prophylaxis in patients undergoing gastrectomy (23), and a recent meta-analysis in surgical patients supported the SDD prophylaxis as a worthwhile maneuver to reduce morbidity and mortality (24). In this study, the SDD prophylaxis was not performed. However, diabetic patients undergoing gastrectomy may be prone to endogenous infections caused by abnormal flora overgrowth in the digestive tract. The SDD may, therefore, be useful for diabetic patients undergoing gastrectomy as an infection prophylaxis.

The retrospective nature of this study may be a limitation. The multivariate analysis was performed to control for the many variables, and DM lasting longer than 10 years was found to have a correlation with the development of postoperative nosocomial infections in diabetic patients undergoing elective gastrectomy. However, the number of studied patients was relatively small because the studied population was restricted to diabetic patients undergoing elective gastrectomy in a single hospital. Although the studied population is rather homogeneous, the statistical power of analysis in this study is reduced. To definitively answer the question whether longer-term DM may be a significant risk factor for the development of postoperative nosocomial infections, a large prospective study would be required.

In conclusion, patients with longer-term DM, especially longer than 10 years, had a significantly greater incidence of postoperative nosocomial infections after elective gastrectomy. Clinicians should consider the DM duration when planning the surgical and perioperative management strategy in diabetic patients undergoing gastrectomy.


   Footnotes
 
Presented in part at the 73rd annual meeting of International Anesthesia Research Society, Los Angeles, CA, March, 1999.


   References
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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Accepted for publication July 20, 2000.




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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins and Stanford University Libraries' HighWire Press®. Copyright 2000 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press