Health care-associated infection (HCAI), previously termed as nosocomial infection 1, is one that is acquired in a hospital or a healthcare facility that was not present or incubating at the time of admission. For most bacterial infections, an onset of symptoms, unrelated to the original illness, which occurs after 48–72 h of admission, is evidence for HCAI acquisition 2.
The significance of HCAI lies not only in its ability to substantially alter morbidity and mortality statistics but also in its economic implications. HCAI prolongs the duration of hospitalization, increases the cost of healthcare, results in the emergence of multiple antibiotic-resistant microorganisms, and reduces the chances of treatment for others 3,4.
Predisposing factors that make patients susceptible to these infections include age of the patient, duration of hospitalization, underlying diseases such as diabetes, concurrent infections, overcrowding in the hospital wards, administration of immunosuppressive agents or broad-spectrum antibiotics, and emergence of multidrug-resistant pathogens 5,6.
Pathogens causing HCAI are acquired from either endogenous or exogenous sources. Endogenous sources are derived from the patient’s own microbial flora following surgical manipulation, chemotherapy, and diagnostic or therapeutic procedures, whereas exogenous sources are derived from the surrounding hospital environment, including another patient or staff member 7.
Skin and soft tissue infections (SSTIs) are caused primarily by Gram-positive pathogens, with Staphylococcus aureus as the predominant pathogen 8. Their clinical management is further complicated by the increasing prevalence of multidrug resistance associated with these infections, including methicillin-resistant Staphylococcus aureus (MRSA) 9,10.
The actual incidence of HCAI is likely to be underestimated as hospital stays may be shorter than the incubation period of the infecting microorganism (a developing infection), and symptoms may not manifest until days after patient discharge 11.
Estimation of the incidence of HCAI in Egypt is challenging because of limited surveillance systems and limited microbiology capacity in some public sector facilities. In addition, the complexity of applying the routine system of reporting infections and the complexity of case definitions hinders the availability of such data. Despite these limitations, some studies indicate that HCAI are emerging as an important public health problem 12.
The present study was carried out to identify the incidence, etiology, and outcome of HCAI in the Dermatology inpatient wards at Cairo University Hospital. The surveillance activities in this study were part of infection control efforts to improve the quality of care.
Patients and methods
We planned this cross-sectional study to determine the incidence and risk factors for HCAI, as well as the antibiotic-resistant bacterial strains in the dermatology inpatient wards at Kasr El Ainy Hospitals, Cairo University. The duration of the study was 3 months from 1 October 2010 to 1 January 2011. During this period, all patients admitted to the wards for a duration of 72 h or more were included in the study. Patients signed informed written consent to participate in this study, which has been approved by the institutional Research Ethics Committee.
Infections occurring during the study period were categorized according to the Centers for Disease Control and Prevention definitions that include clinical and laboratory criteria 13. To classify an infection as HCAI, it must be clear that it was not present or in incubation at the time of the patient’s admission.
For each patient, the following was performed
Full medical and dermatological history, thorough medical and dermatological examinations, observation of general and local signs of infection, body surface area (BSA) affection using the rule of nines 14, documentation of other medical conditions, particularly diabetes, hypertension, liver or renal disease, history of surgical operations, and malignancy, recording of the presence of invasive devices such as a peripheral venous line, urinary catheters, or nasogastric tubes, detailed drug history with an emphasis on antibiotics, immunosuppressive medications, corticosteroids, and chemotherapy, and recording the duration of stay.
The dermatology inpatient department at Kasr El Ainy Hospital includes a large ward containing 24 beds for female patients and two smaller wards for male patients, each containing eight beds. In addition, it contains two isolation rooms for indicated cases, each containing two beds.
Beds are separated from each other by a distance of 1 m. In the dermatology wards, the nurses work three (eight hourly) shifts. In the morning shift, five nurses serve patients, whereas in the evening and night shifts, only one nurse serves patients.
The nurse-to-patient ratio for the morning shift (when most of the medications are administered, investigations and procedures are performed, and patient care is provided) is 1 : 8 and was used in this study. During evening and night shifts, the nurse-to-patient ratio reaches 1 : 40, because of shortage of trained nurses in the dermatology wards. Using alcohol and washing hands with antiseptic soaps were the main techniques used for disinfection by the nurses and staff.
Samples were obtained from skin lesions upon admission and after 72 h. The study wards were visited daily; nursing notes, medical notes, microbiology reports, temperature charts, and antibiotic treatment charts were reviewed to determine whether a patient had symptoms and/or signs of infection. A worksheet for every inpatient (infected and noninfected) hospitalized for more than 72 h was filled.
Various clinical samples from suspected infected sites: skin, wound, conjunctival secretion, urine, sputum, and tip of the intravenous cannula, were obtained and processed as per the standard microbiological procedures 15,16. This was followed by the use of conventional methods for the identification and characterization of the isolates 17. All pathogenic isolates were then tested for their in-vitro susceptibility to various commercially prepared antimicrobial discs (Oxoid, Ogdensburg, New York, USA) using the disc diffusion method on Mueller–Hinton agar plates (Oxoid) according to the Clinical and Laboratory Standards Institute guidelines 18.
Data were statistically described in terms of mean±SD and minimum and maximum of the range for numerical parametric data; as median and first and third interquartile range for numerical nonparametric data; and as number and percentage for categorical data. Inferential analyses were carried out for quantitative variables using an independent t-test in cases of two independent groups with parametric data and Mann–Whitney U-test in cases of two independent groups with nonparametric data. Inferential analyses were performed for qualitative data using the χ2-test for independent variables. The significance level was set at P value less than 0.05. Statistical analyses were performed using a software package (SPSS) software version 18.0 (SPSS Inc., Chicago, Illinois, USA).
Demographic clinical results
A total of 180 admissions were recorded during the study period. These patients were 55 men (30.6%) and 125 women (69.4%). The mean age of the patients was 42.2 (±15.2) years, ranging from 15 to 71 years. All patients in the wards had an intravenous cannula, with no other medical device reported. The nurse-to-patient ratio in the study period was one nurse to eight patients.
According to the medical history, 53 patients (29.4%) had diabetes mellitus, 30 patients (16.7%) had hypertension, and 29 patients (16.1%) had liver disease.
The criteria for HCAI were fulfilled in 10 patients (5.6%), yielding an incidence of 5.6 HCAI per 100 patients. Urinary tract infections were documented in four cases (2.2% of all cases), SSTIs were found in three cases (1.7%) (one case developed SSTI following the removal of a cannula, the other two cases developed SSTIs in the gluteal region at the site of intramuscular injection), conjunctivitis was detected in two cases (1.1%), and respiratory tract infection in one case (0.6%). The primary diagnoses of 180 patients and the type of HCAI in a total of 10 cases are presented in Table 1.
The BSA involvement of the skin lesions in the HCAI patients ranged from 15 to 90%, with more than an 85% involvement in seven cases. The length of stay (LOS) in the hospital of the patients who developed HCAI ranged from 10 to 50 days, with a median of 40 days, whereas in the non-HCAI group, it ranged from 4 to 65 days, with a median of 5 days, with a statistically significant difference (P<0.001). The course of the skin disease was progressive in seven HCAI patients (70%), whereas in the non-HCAI group, it was progressive in 27 (15.9%), (P<0.001). Prior antibiotic treatment was administered in the 10 patients who developed HCAI (100%), whereas it was administered in only 29 patients (17.1%) of the non-HCAI group (P<0.001). No significant difference was found between the HCAI group and the non-HCAI group in terms of personal history [e.g. age, sex, smoking, and residence area (urban/rural)], medical conditions (e.g. diabetes, hypertension, liver or renal disease, history of surgical operations, and malignancy), and intake of immunosuppressive medications, steroids, and chemotherapy. Relevant present history data of the studied cases are presented in Table 2.
The most frequently isolated pathogenic microorganism was S. aureus (60%), followed by Escherichia coli (10%). In the remaining three cases (30%), the specimens (all urine) showed no growth. On sensitivity testing, 83.3% of S. aureus (five cases) were MRSA and only 16.6% (one case) were methicillin-sensitive Staphylococcus aureus (Fig. 1).
In the present study, the two patients with the HCAI conjunctivitis were in the same ward and developed the infection at the same time. Isolated organisms in both cases were MRSA. A third MRSA-infected case was diagnosed with an SSTI during the same week in a different ward in the dermatology inpatient. Also, two patients with urinary tract infection in whom no growth was obtained in culture were diagnosed in different rooms at the same time. The remaining five cases of HCAI developed the infection at different times and in separate wards.
On testing for the antibiotic sensitivity of HCAI cases, all cases of MRSA were sensitive to vancomycin and rifampicin. Four cases were sensitive to cotrimoxazole and three cases were sensitive to ciprofloxacin and levofloxacin. However, they were all resistant to ampicillin, amoxicillin clavulanate, fusidic acid, oxacillin, and gentamycin. The methicillin-sensitive Staphylococcus aureus case showed resistance only to clindamycin and erythromycin.
The HCAI mortality was one out of 10 patients at a 10% rate. This patient was a 45-year-old man with pemphigus vulgaris; MRSA growth was obtained from the conjunctival mucosal surface. He was on oral mycophenolate mofetil and intravenous corticosteroid pulse therapy. However, his disease followed a progressive course and was nonresponsive to therapy. His skin and blood cultures were negative and the cause of death in this case was extensive skin lesions involving over 90% of BSA with a progressive course resistant to treatment, electrolyte imbalance, hypoalbuminemia, and dehydration.
According to this work, we detected a total of 10 HCAI in 180 hospitalized patients in the dermatology ward over a period of 3 months, indicating an incidence of HCAI of 5.6%. The overall incidence of HCAI in developed countries varies between 5.1 and 11.6%. The estimated HCAI incidence rate in the USA was 4.5% in 2002 19. The European Centre for Disease Prevention and Control reported an average incidence of 7.1% in European countries 20.
Parallel to the findings of Lim et al.21, we found that the LOS was significantly longer in patients who developed HCAI compared with those without HCAI, as the median LOS in HCAI patients was 40 days, whereas it was 5 days in the non-HCAI group, and in 70% of patients developing HCAI, the LOS exceeded 30 days. Prolonged LOS in hospitals, which is usually linked to disease severity, leads to increased medical interventions that eventually result in an increased incidence of HCAI 22.
In our study, a progressive disease course was detected in 70% of patients developing HCAI, whereas it was only detected in 27% of the patients in the non-HCAI group, with a statistically significant difference. Moreover, 70% of NI cases had extensive skin lesions with more than 85% of the BSA affected, assumed to result in infection, electrolyte imbalance, and even death 23.
In the present work, prior antibiotic therapy was administered in 100% of patients who developed HCAI compared with 17.1% in the non-HCAI group. According to the policy regarding antibiotic usage followed in our inpatient ward, any patient with active skin lesions or any patient who develops noncutaneous infection receives an empirical broad-spectrum antibiotic for 1 week such as a third-generation cephalosporin, amoxicillin clavulanate, or ampicillin/sulbactam according to availability in the pharmacy and without special preferences.
In the present work, S. aureus was the causative organism in six cases, of which five cases (83.3%) were caused by MRSA. The prevalence of MRSA has increased worldwide, and the highest rates have been found in developed countries 24. In the USA, ∼60% of S. aureus infections are caused by MRSA 25.
A previous work detected increasing antibiotic resistance among patients hospitalized for dermatologic conditions, specifically MRSA 26. It has been reported that most HCAIs develop because of multidrug-resistant pathogens and result from the administration of empirical broad-spectrum antibiotics before identification of the etiologic agents 27, comparable with the current practice of antibiotic administration in the dermatology wards. Overuse of antibiotics further contributes to an increase in multidrug resistance 27. Moreover, in 30% of our HCAI cases, cultures yielded no bacterial growth, which may be related to the routine followed, but may possibly because of nonbacterial pathogens.
In the present study, all cases of MRSA were resistant to ampicillin, amoxicillin clavulanate, fusidic acid, and oxacillin. Similarly, in the UK, Shah and Mohanraj 28 detected a high level of fusidic acid resistance to 50% of S. aureus isolated from dermatology outpatients, which increased to 78% in inpatients with atopic dermatitis.
In the present study, the two HCAI cases with HCAI conjunctivitis developed in the same ward, and their culture revealed MRSA. They were subsequently isolated in a separate hospital room. During the same week, a third HCAI case of SSTI also revealed MRSA, but in a different dermatology ward. Possible transmission mechanisms include direct contact, foments, or from attending staff.
The hospital infection control committee was informed about each case of MRSA, for which an infection control practitioner was assigned for staff education and training on infection control measures to reduce cross contamination. Furthermore, environmental cleanliness was carried out by appropriate disinfection practices for all the ward surfaces.
The nurse-to-patient ratio during our study period was 1: 8. This low nurse staffing leads to a higher workload. The Centers for Disease Control and Prevention data 29 indicate that understaffing may be a risk factor for nosocomial infections. When the patient-to-nurse ratio increases, routine nursing measures such as compliance with aseptic techniques may decrease. This is associated with an increased risk of complications in patients, and increasing the nurse-to-patient ratios has been recommended as a means to improve patient safety 30. Strict adherence to conventional measures such as hand hygiene, aseptic precautions, appropriate sterilization, and disinfection practices can contribute considerably toward reducing HCAI 31. Nurses have the unique opportunity to directly reduce HCAI by recognizing and applying evidence-based procedures to prevent these infections among patients and protect the health of the staff 32.
The present study documents for the first time, to our knowledge, the incidence of HCAI in an Egyptian university hospital dermatology ward. We conclude that increased hospital LOS of patients, progressive course of disease, empirical use of broad-spectrum antibiotics, and a low nurse-to-patient ratio were the main causes for development of NI. Our data suggest that the incidence of HCAI in dermatology ward, 5.6%, appears to be within the reported international levels; however, this value can be reduced by addressing the predisposing factors.
Conflicts of interest
There are no conflicts of interest.
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