Surgical infections (SIs) are infections of the tissues, organs or spaces, exposed by surgeons during performance of an invasive procedure. The development of SIs is related to 3 factors; the degree of microbial contamination of the wound during surgery, the duration of the procedure and host factors, such as diabetes, malnutrition, obesity, immunosuppression, and the number of other underlying disease states.1
SIs are associated with considerable morbidity and occasional lethality, as well as substantial healthcare costs and patient inconvenience and dissatisfaction.2 For that reason surgeons strive to avoid SIs by the use of mechanical, chemical and antimicrobial modalities, or a combination of these methods for prophylaxis.
Bacteria are responsible for the majority of surgical infections. Gram-positive bacteria that frequently cause infections in surgical patients include aerobic skin commensals and enteric organisms. There are many pathogenic gram-negative bacterial species that are capable of causing surgical infections, predominantly members of the Enterobacteriaceae family. Anaerobic bacteria, fungi, and viruses are the other causes of SIs. Fungi cause nosocomial infections in surgical patients as a part of polymicrobial infections or fungemia, rare causes of aggressive soft tissue infections and so-called opportunistic pathogens.1
The aim of this study was to evaluate the fungal agents as a cause of SIs, and to discuss the host factors predisposing the infection.

Methods

The study was carried out in the laboratory of Microbiology Department of Medical Faculty of Duzce University. Culturing results of surgical wound infections between January 2001 and December 2005 were evaluated. A total of 824 samples were sent to the laboratory from surgical clinics during this period.
The specimens were obtained by using sterile swabs and immediately inserted in Dio-Transport swab/Stuart medium (Diomed Inc, Istanbul, Turkey) and sent to the laboratory. All samples were inoculated onto 5% sheep blood agar, Eosin Methylene Blue (EMB) agar and Sabouraud Dextrose Agar (SDA)’s and Gram, EZN and Giemsa staining procedures were applied for all samples. Plates were incubated for 24–48 hours and than examined. Growth was obtained and conventional microbiological methods and the API System (bioMérieux, Marcy l’Étoile, France) were used to identify the organism. The results were interpreted parallel to the staining results.

Results

A total of 824 samples including all submitted surgical specimens were evaluated and organisms were recovered from 455 (55.2%) of the samples. Of 455 isolates, 443 (97.4 %) were bacteria, 12 (2.6%) were fungi, 47 (10.3%) bacteria, and 9 (2%) fungi were isolated as the cause of SIs. Fungal growth was obtained as pure cultures. As a result of identification of these fungi, all were yeasts. Five (55.6%) were identified as Candida albicans, 3 (33.3%) as Candida tropicalis, and 1 (11.1%) as Candida glabrata.
Fungal growth was obtained in 9 specimens of the patients who have at least 1 predisposing factor to fungal infections. Two of these patients had died as a result of fungemia, which was diagnosed by the growth of fungi in blood cultures. Of these patients, 5 had cancer, 1 was receiving chemotherapy, and 4 were terminally ill. Two patients from the intensive care unit had head injuries, and a body mass index (BMI) under 15 kg/m2, and 2 patients had type 2 diabetes mellitus. All of the patients were receiving prophylactic antimicrobial therapy. Characteristics of the patients were listed in Table 1.

Discussion

Surgical infections result in significant increases in mortality, length of hospital stay, and healthcare costs. Virulence of the microbial agents, host resistance, and factors about the wound are the determinants of the infection after surgery. Risk factors related to patients for development of SIs are older age, immunosuppression, obesity, diabetes mellitus, chronic inflammatory process, malnutrition, peripheral vascular disease, anemia, radiation, chronic skin disease, carrier state of organisms, and recent operation.1
Patients with cancer have increased risk of developing an infection related directly to cancer and/or cancer treatment. Damage of the skin and mucous membranes, impairment of the immune system, tumor-associated abnormalities, nutrition, surgery, receiving chemotherapy and radiation therapy, and psychological factors all play a role in the development of infection.3 Immunosuppression may result from the use of corticosteroids, chemotherapy, radiation therapy, surgery, hematopoietic stem cell transplantation, or the cancer itself. The growth of tumors can disrupt natural barriers, invade and replace the normal cells in the bone marrow, compress nearby normal tissues, and can reduce blood flow or cause an obstruction. Cancer cells can also release substances that interfere with the proper functioning of immune system cells, especially if they are large and have spread extensively.3
Dietary factors, such as decreased intake of vitamins, minerals, calories, and protein can alter immune function. As a result of cancer treatments, decreased appetite, nausea, and poor nutrition makes the immune system less effective in recognizing and destroying organisms. Today, researchers have shown that people with cancer experiencing higher levels of stress tend to be at greater risk for infection, but the relationship of psychological factors to infection is not completely understood.3
The role of major surgery as a cause of immunosuppression also is not clearly defined. Within hours of surgery researchers have noted decreases in immune function. Anesthetic agents, disruption of the skin and mucous membranes, the length of hospitalization, the extent of the surgery, the duration of the operation, the amount of bleeding during surgery, the nutritional state of the person, prior cancer treatment of the surgical area, prophylactic antibiotics, and other medical problems are the factors that increase the risk of infection after surgery. As surgery is a common treatment for people with cancer, it is important to be aware of infection risk after surgery.3
People with cancer may develop several types of infections by organisms that are normally present in the environment and people's bodies. These opportunistic infections are related to the weakened defenses of patients. Common causes of fungal infections in cancer patients are predominantly Candida spp, followed by Aspergillus, Cryptococcus, Histoplasma, Phycomycetes, and Coccidioides. These infections can be serious, and in some cases, fatal. Of the patients reviewed in the present study, 5 had malignancies including bladder, stomach, and colon carcinomas. Candida albicans was the fungi predominantly isolated from abdominal incision specimens. Relation between cancer and fungi seem to reflect to the results of our study, as about half of the patients are of this group and the distribution of the isolates was similar to literature.3
Nutrition is a critical determinant of immune responses and malnutrition the most common cause of immunodeficiency worldwide. Protein-energy malnutrition is associated with a significant impairment of cell-mediated immunity, phagocyte function, complement system, secretory immunoglobulin A antibody concentrations, and cytokine production.4 Patients with head injury suffering from severe malnutrition exhibit serious complications at the time of admission as well as during rehabilitation treatment.5 Two patients with head injuries were severely malnourished and had a BMI < 15 kg/m2. These patients were receiving antibiotherapy, had had a long stay in the intensive care unit, and instrumented—these were all risk factors for acquiring infection aside from malnutrition.
Endocrine diseases such as diabetes mellitus, Cushing syndrome, hypoparathyroidism, hypothyroidism, and polyendocrinopathy are associated with increased susceptibility to infection.6 The reasons why diabetic patients present with an increased susceptibility to frequent and protracted infections remain unclear. The mechanism by which diabetes mellitus is believed to raise infection rates is through increased tissue glucose, altered yeast adhesion, and decreased phagocytosis.6 Studies demonstrated immune abnormalities in vitro models. The participation of genetic and autoimmune factors has been mainly characterized on T lymphocyte function, opsonization defects, the depletion of memory CD4+ cells and the defective natural killer activity could transiently impair host defenses. Several in-vitro functional defects of the immune system have been correlated with the metabolic control of diabetic patients. The importance of systemic consequences of insulinopenia, such as hyperglycemia and ketosis, has also been addressed. Recent studies have shown abnormalities of signal transduction mechanisms in which insulinopenia and other factors, such as circulating immune complexes, could be involved.7
Clinicians and researchers are linking elevated glucose levels with potential infectious outcomes.8 Physiologic processes to fight foreign agents are potentially impaired during periods of hyperglycemia. Immune function and the inflammatory response, for example, are impaired when they are needed most (eg, during recovery from surgical procedures).8 Despite numerous controversies, many in-vitro studies of the immune cells of patients with diabetes have demonstrated significant defects that bear quantitative similarities with abnormalities described in other immunodeficiency syndromes.7 In the present study, 2 patients were elderly and had type 2 diabetes mellitus. Candidal growth in this group can be explained as a result of immunodeficiencies related to endocrine diseases.
Antibiotic use is another factor that influences the acquirement of fungal infections. Antibiotics damage the ecology of microorganisms in the bowel and on body surfaces, permitting the overgrowth of Candida and undesirable bacteria.9 Most patients in the present study received prophylactic broad-spectrum antibiotics before and after surgery. This factor seems to cause more susceptibility to fungal infections, in addition to other factors.

Conclusion

All patients in this study with fungal overgrowth of surgical wound specimens had one or more predisposing factors that impaired their immune system, especially cell-mediated immunity. As immunosuppression is a risk for fungal infections, and fungal infections represent one of the most rapidly increasing health care infections coupled with a significant mortality rate,10 clinicians must be aware of fungal infections that may develop in this at-risk group, particularly after surgery involving older adults and pediatric patients.
The results reflect infections due to Candida species acting as an etiologic agent. In the last 2 decades the incidence of Candida infection has shown a shift from Candida albicans to other Candida species.11–16 Changing epidemiologic patterns has seen the emergence of nonalbicans strains13 often associated with resistance to azole antifungal agents,14 which has implications on patient management. Recently published standards of care15 advocate that all Candida species isolated from sterile sites and all species from high-risk patients should be identified at the species level.17