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Prevalence of hospital-acquired infections and antibiotic use in two tertiary Mongolian hospitals
Journal of Hospital Infection 75 (2010) 214–219
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Journal of Hospital Infection journal homepage: www.elsevierhealth.com/journals/jhin
Prevalence of hospital-acquired infections and antibiotic use in two tertiary Mongolian hospitals B.-E. Ider a, *, A. Clements a, b, J. Adams a, M. Whitby c, T. Muugolog d, e a
University of Queensland, School of Population Health, Brisbane, Queensland, Australia Australian Centre for International and Tropical Health, Queensland Institute of Medical Research, Brisbane, Queensland, Australia c Infection Management Services, Princess Alexandra Hospital, Brisbane, Queensland, Australia d Hospital Related Infection Surveillance and Research Unit, National Center for Communicable Diseases, Ulaanbaatar, Mongolia e Mongolian Association of Infection Control Professionals, Ulaanbaatar, Mongolia b
a r t i c l e i n f o
s u m m a r y
Article history: Received 24 August 2009 Accepted 13 January 2010 Available online 1 April 2010
Health statistics of Mongolia indicate that hospital-acquired infections (HAIs) occur in 0.01–0.05% of all hospital admissions. This is considerably lower than internationally reported rates. A one-day survey was conducted in two tertiary hospitals of Ulaanbaatar in September 2008 to estimate HAI prevalence, associated risk factors and patterns of antibiotic usage. Among 933 patients surveyed, 50 (5.4%) were diagnosed with HAI. Prevalence of surgical site infection was 1.1% (3.9% among surgical patients), bloodstream infection 0.3%, respiratory tract infection 1.3%, urinary tract infection 1.3%, and other HAI 1.4%. Microbiological investigations were only documented for 18.9% of all patients. A total of 558 patients (59.8%) were taking 902 courses of antibiotics; 92.1% of patients were prescribed antibiotics without a sensitivity test. Multiple logistic regression analysis revealed that HAI was significantly associated with the admission source, the hospital, length of hospital stay, surgical and other invasive procedures, urinary catheters and other indwelling devices. The study results were comparable with reports from some other developing countries and confirm that official statistics underestimate the true frequency of HAI in Mongolia. Ó 2010 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved.
Keywords: Hospital-acquired infection Mongolia Point prevalence study Prevalence Risk factors Under-reporting
Introduction As a consequence of the rapid political and structural changes that occurred in Mongolia in the early 1990s, the strong Sanitary Epidemiological Service that had been inherited from the socialist government was dismantled without replacement.1 Plans were adopted by the new, democratically elected government to reorganise the public health system, and these included a strategy for hospital infection control.2,3 However, implementation has been slow for a myriad of reasons, including resource limitations and a lack of expert personnel.4 A Hospital Related Infection Surveillance and Research Unit (HRISRU) has been established at the National Centre for Communicable Diseases (NCCD) in the capital city, Ulaanbaatar.5 The HRISRU has been collecting hospital-acquired infection (HAI)
* Corresponding author. Address: University of Queensland, School of Population Health, Australia. Tel.: þ61 73346 4829; fax: þ61 73365 5442. E-mail address: [email protected] (B.-E. Ider).
surveillance data since 1998 from all tertiary and secondary level hospitals. The reported prevalence of HAI has been 0.01–0.05% of all hospital admissions, with the highest prevalence (0.05%) reported for tertiary hospitals in Ulaanbaatar.6,7 Other than the HRISRU reports, there have been no published HAI prevalence studies from Mongolia. Meanwhile, other studies have shown that HAI prevalence varies from 3.5% to 13.8% in high income industrialised countries, and from 4.9% to 22.4% in middle and low income countries.8–23 The low observed rate of HAI in the HRSIRU reports is almost certainly due to considerable under-reporting. There are many potential reasons for under-reporting which are not the focus of this study. Accurate data on the burden of HAI are essential for resource planning and the formulation of policies and guidelines for infection control and surveillance. To address this need, we aimed to determine the first accurate estimate of overall HAI prevalence, as well as prevalence of internationally recognised types of HAI, in two tertiary hospitals of Ulaanbaatar. We also aimed to identify risk factors for HAI among patients in those hospitals, to provide evidence for future HAI control programmes.
0195-6701/$ – see front matter Ó 2010 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2010.01.016
B.-E. Ider et al. / Journal of Hospital Infection 75 (2010) 214–219
Methods Setting The two largest tertiary teaching hospitals in Ulaanbaatar as defined by service features and bed capacity, hereafter referred to as hospitals A and B, were chosen for the study. Hospital A has 544 beds and a bed occupancy of 75.7%. It has 14 departments (six surgical, seven medical and one intensive care/emergency unit), providing care for adults only. Hospital B has 733 beds with a bed occupancy of 71.9% and has 25 departments (six surgical, 12 medical, seven intensive care/emergency units). It delivers tertiary medical services to paediatric, obstetric and gynaecology patients. Ethical considerations and study population Ethical approval for the study was obtained from the National Medical Research Ethics Committee of Mongolia and the Medical Research Ethics Committee of the University of Queensland, Australia. All 940 inpatients in the hospitals on the study day, or a legal proxy, were asked to provide consent to participation and only seven patients (0.7%) refused. Definitions The current infection control guidelines in Mongolia lack standardised definitions for HAI. Therefore the US Centres for Disease Control and Prevention (CDC) definitions of HAI, widely utilised in similar studies, were used in the study for standardisation and comparison purposes.8,10,11,15–17,20–22,24,25 These categorise 41 diagnostic groups which were classified as: (1) surgical site infection (SSI), (2) bloodstream infection (BSI), (3) urinary tract infection (UTI), (4) respiratory tract infection (RTI) and (5) other infection. All infections with onset >48 h after admission were recorded as HAI. SSI in surgical patients who were readmitted due to infection within one month of surgery or within one year after an implant was placed, were also classified as HAI. Surgical patients with a clean or clean-contaminated wound class and who had symptoms of infection were recorded as having HAI.26 Patients with a contaminated or dirty-infected wound class were classified as having a community-acquired infection (CAI) together with all other infections. Antibiotic therapy was defined as prophylactic when it was prescribed to patients who had no progressive infections, including infectious comorbidities. Pilot study A pilot study was conducted in one general hospital of Ulaanbaatar to test and refine the survey methods. Eighteen infection control practitioners (ICPs) were recruited from tertiary and secondary level hospitals of Ulaanbaatar and the HRISRU for the pilot study. Data collection A one-day prevalence study was conducted during two consecutive weeks: the weeks starting 30 September 2008 in hospital A and 8 October 2008 in hospital B. On the study day, each of the 18 ICPs was designated 20–30 patients in surgical departments, intensive care and emergency units (IC&EU) or 30–40 patients in obstetrics and gynaecology (O&G), and medical departments. Data were recorded from each patient’s records, ward’s laboratory results and nursing books. Data included: hospital and department name, date of birth, gender, admission date and time, admission purpose (diagnostic or treatment), admission mode
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(emergency or planned), admission source (home, other hospital/ department, or born in hospital), admission diagnosis, comorbidities (premature birth, diabetes, chronic respiratory and cardiovascular diseases, immunocompromise (including chemotherapy, hormone or radiation therapy, acquired immune deficiency syndrome), antibiotic usage (name, duration and purpose), microbiological tests (sites, isolates and antimicrobial susceptibility), body temperature, laboratory results (leukocyte count, erythrocyte sedimentation rate, C-reactive protein and urine sediment) and radiography results. Presence of indwelling devices during the current hospital stay was recorded. The devices were categorised as: mechanical ventilation devices, central and peripheral venous catheters, urinary catheters, wound drains and other devices (including epidural catheters and nasogastric tubes). All surgical procedures and operations undergone during the previous 30 days and surgical prostheses placed during the previous 12 months were also noted. After transferring data to the data collection forms, the ICPs visited the wards to conduct patient examinations, where they determined whether patients belonged to one of three groups: patients with no infection, patients with HAI and patients with CAI. At the bedside, ICPs asked patients if they were experiencing specific clinical symptoms of infection (e.g. fever, shivering, chills or malaise). Patients were also asked to show the ICP any surgical wounds and catheter sites. Occurrence of HAI or CAI, as defined above, was recorded. Statistical analysis The statistical software packages SPSS 15.0 (SPSS Inc, Chicago, IL, USA) and STATA-10 (Stata Corp LP, College Station, TX, USA) were used in the analysis. Initial descriptive summary statistics were calculated. The CAI data were not analysed further, but a subsequent analysis was conducted to determine risk factors for HAI, with the patients from both hospitals grouped together. Explanatory variables were divided into those that were intrinsic and extrinsic to the patient. Bivariable analyses were performed using cross-tabulation and logistic regression methods. Odds ratio (OR), 95% confidence interval (95% CI) and P-value were estimated for each intrinsic and extrinsic variable. Explanatory variables with P < 0.2 were considered as candidates for subsequent multivariable models. The candidate variables were tested for multicolinearity and variables found to be colinear with other variables (as defined by a variance inflation factor >10) were removed. Backward stepwise logistic regression models were run for intrinsic (model I), extrinsic (model II) and both intrinsic and extrinsic (model III) groups of explanatory variables using an exit criterion of P > 0.2 and an entry criterion of P 0.1. Results Patient features Of the 933 surveyed patients, 423 (45.3%) were men and 510 (54.7%) were women. The mean age was 26.5 years (SD: 22.1; range: 0–93); 45.2 years in hospital A (N ¼ 405) and 12.2 years in hospital B (N ¼ 528). The mean length of stay from admission to study day was 5.7 days (range: 0–76; median: 5). Of these, 299 were surgical, 398 were medical, 160 were O&G and 76 were IC&EU patients. A total of 138 patients (14.8%) had a total of 275 indwelling devices. Peripheral venous catheters were the most common (142) followed by epidural catheters and nasogastric tubes (46), wound drains (41), urinary catheters (32), central venous catheters (9) and endotracheal tubes (5). Device utility levels were similar in both
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hospitals (13.6% and 15.7% for hospitals A and B respectively). Seventy-six patients had one device, 39 had two, nine had three, and 14 had four or more devices. In total, 253 (27.1%) patients had undergone 273 surgical episodes; 239 patients had one operation, ten patients had two, two patients had three, and two patients had four. The most common wound class was clean-contaminated, 146 (53.5%) patients, followed by dirty-infected wounds, 55 (20.1%) patients. The surgical site class composition was similar in the two hospitals. Infections Of 933 patients, 343 (36.8%) had an infection during their hospital stay (Table I). Of these, 293 patients were diagnosed with CAI and 50 with HAI, providing a crude prevalence of 31.4% for CAI and 5.4% for HAI. No patients were diagnosed as having two or more HAIs. Among HAIs, the most common infections were skin and tissue infections (grouped as ‘others’) (1.4%), followed by respiratory tract (1.3%), urinary tract (1.3%), surgical site (1.1%) and bloodstream (0.3%) infections. Hospital A had 15 HAI cases with an overall prevalence of 3.7%, whereas hospital B had 35 HAI cases with an overall prevalence of 6.6%. The prevalence of SSI among surgical patients was 2.4% (3/126) for hospital A, 5.5% (7/127) for hospital B and 3.9% (10/253) overall. Approximately two-thirds of SSI were deep or organ space infections.
Table I Infection outcomes among patients surveyed in two tertiary hospitals in Ulaanbaatar, Mongolia, 2008 Main variables
Hospital A
Hospital B
Patients with infectionsa Community-acquired infection (CAI) Hospital-acquired infection (HAI) HAIs by departmentb Surgical Medical Obstetrics and gynaecology Intensive care and emergency Types of HAIa Surgical site infection Bloodstream infection Urinary tract infection Respiratory tract infection Others List of HAIsa Incisional surgical wound infection Deep surgical wound infection Laboratory-confirmed bloodstream infection Clinical sepsis Symptomatic urinary tract infection Pneumonia Bronchitis, tracheobronchitis, bronchiolitis, tracheitis, without evidence of pneumonia Meningitis or ventriculitis Gastroenteritis Intra-abdominal infection Conjunctivitis Upper respiratory tract infection (pharyngitis, laryngitis, epiglottitis) Joint or bursa infection Skin infection (other than incisional wound infection) Soft tissue infection Breast abscess or mastitis Omphalitis in newborn
123 (30.4) 108 (26.7) 15 (3.7)
220 (41.6) 185 (35.0) 35 (6.6)
343 (36.8) 293 (31.4) 50 (5.4)
9 (4.9) 4 (1.9) – 2 (40.0)
6 (5.3) 14 (7.7) 6 (3.8) 9 (12.7)
15 (5.0) 18 (4.5) 6 (3.8) 11 (14.5)
3 (0.7) – 8 (2.0) 4 (1.0) –
7 3 4 8 13
10 3 12 12 13
(1.3) (0.6) (0.8) (1.5) (2.5)
2 (0.5) 1 (0.2) –
1 (0.2) 6 (1.1) 1 (0.2)
– 8 (2.0) – 1 (0.2)
2 (0.4) 4 (0.8) 5 (0.9) –
– – – – 3 (0.7)
2 1 1 3 3
(0.4) (0.2) (0.2) (0.6) (0.6)
Total
(1.1) (0.3) (1.3) (1.3) (1.4)
3 (0.3) 7 (0.8) 1 (0.1) 2 12 5 1
(0.2) (1.3) (0.5) (0.1)
2 1 1 3 6
(0.2) (0.1) (0.1) (0.3) (0.6)
– –
1 (0.2) 1 (0.2)
1 (0.1) 1 (0.1)
– – –
1 (0.2) 1 (0.2) 2 (0.4)
1 (0.1) 1 (0.1) 2 (0.2)
Values in parentheses are percentages. a Denominator is the total number of patients. b Denominator is total number of patients in this group of departments.
Microbiological testing Of all patients, 176 (18.9%) had 233 (including seven missed) culture tests. Of these, 146 (83.0%) patients had one and the remaining 30 (17.0%) had repeated microbiological tests (up to six times) during their hospital stay. Cultures from the urine (50.4%), skin including eye, ear and vagina (16.4%), and surgical wound (11.5%) were the most common. Among 226 cultures, 137 (60.6%) yielded no pathogens and for 6 (2.7%) the results were pending at the time of the study, leaving 83 (36.7%) from which a pathogen had been isolated. The most common pathogens were Escherichia coli (31.3%) and Staphylococcus aureus (20.5%). In hospital A these pathogens were isolated from 33.3% and 36.4% of all cultures respectively. Among 50 patients diagnosed with HAI, 23 (46.0%) had documented microbiological results. Cultures were taken from urine (14), blood (8), swabs other than surgical wound (7), surgical wound (4), sterile fluids (3) and sputum (1). Isolated micro-organisms were E. coli (7), S. aureus (4), Enterobacter spp. (3), Enterococcus spp. (1), Proteus mirabilis (1), Candida spp. (1) and, in one case, an unidentified cocci on vaginal smear (1). Antibiotic use A total of 558 (59.8%) patients were taking 902 courses of antibiotics with the average number of antibiotics per patient being 1.62 (SD: 0.88; range: 1–6). In hospital A, 208 (51.4%) patients were taking 308 antibiotic courses with an average of 1.48 (SD: 0.75; range: 1–5) antibiotics per patient, whereas in hospital B, 350 (66.3%) patients were taking 594 courses with an average of 1.70 (SD: 0.94; range: 1–6) antibiotics per patient. At the time of the study, the mean duration of antibiotic therapy was 3.63 days (SD: 2.47; range: 0–14; median: 4.0) in hospital A, 3.71 days (SD: 3.21; range: 0–22; median: 3.0) in hospital B, and 3.68 days (SD: 2.90; range: 0–22; median: 3.0) overall. Twenty-two types of antibiotic were administered to patients, the most common being ampicillin, gentamicin and cefazolin, together accounting for 72.2% of all antibiotics administered. The most commonly prescribed antibiotics were a combination of ampicillin and gentamicin in hospital B and sole administration of cefazolin or ampicillin in hospital A. A total of 567 (64.9%) antibiotic courses were prescribed for treatment of infections. Ampicillin (27.0%), cefazolin (22.2%), gentamicin (20.6%), metronidazole (6.9%) and penicillin (4.2%) were the most frequently prescribed. The other 306 (35.1%) courses were prescribed for prophylactic purposes, mainly for surgical patients, patients with trauma or immunocompromised patients including cancer patients and preterm newborns. Ampicillin (40.5%), gentamicin (21.2%), cefazolin (15.0%), metronidazole (4.9%) and cefotaxime (3.9%) were the most commonly prescribed antibiotics for prophylaxis. Among 50 patients diagnosed with HAI, 47 (94.0%) were being administered antibiotics with an average number of antibiotics of 2.30 (SD: 1.19; range: 0–6) per patient. At the time of the study, the mean duration of antibiotic treatment was 5.74 days (SD: 4.51, range: 0–22; median: 5.0). These patients received a total of 107 antibiotic courses, with the most common being gentamicin (22), ampicillin (21), cefazolin (19), metronidazole (12) and cefotaxime (10). As elsewhere in Mongolia, the manual disc diffusion method is the only method of antibiotic susceptibility testing in these two hospitals. Commercially available discs for 12–15 commonly prescribed antibiotics are used. Fifty-one (5.5%) patients had a total of 70 antibiotic sensitivity tests conducted on bacterial isolates during their hospital stay, which represents 7.9% of those patients being administered antibiotics. The remaining 92.1% of patients were administered antibiotics without a sensitivity test being done, including 80.0% of patients diagnosed with HAI.
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For 70 tests conducted, sensitivity was assessed for 15 types of antibiotic. The antibiotics to which most pathogens were sensitive included cefotaxime (47.1%), ciprofloxacin (21.4%), ceftriaxone (15.7%), gentamicin (15.7%) and cefazolin (14.3%). In hospital A, the antibiotics to which most pathogens were sensitive were cefotaxime (68.7%) and ciprofloxacin (40.6%); in hospital B, they were cefotaxime (29.0%) and cefazolin (23.7%). HAI risk factors Among intrinsic factors, the patient’s age, admission mode, admission source, premature birth and presence of other allied conditions were found to be significantly associated with HAI in the bivariable analysis. Among extrinsic factors, hospital, department, patient’s length of hospital stay, surgical and other invasive procedures, indwelling device (mechanical ventilation, central and peripheral intravascular cannulas, urinary and other catheters) and
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number and duration of indwelling devices were significantly associated with HAIs in the bivariable analysis. In the multivariable model with intrinsic risk factors, only four variables had P < 0.2: patient age, admission mode, admission source, and premature birth (Table II). In the model with extrinsic factors, six variables had P < 0.2: hospital, length of hospital stay, surgical and other invasive procedures, use of peripheral intravascular, urinary catheters and other indwelling devices. In the overall model, with both intrinsic and extrinsic factors, six factors were significant: admission source, hospital, length of hospital stay, surgical and other invasive procedures, urinary catheters and other indwelling devices (i.e. epidural catheters and nasogastric tubes). Discussion We found that the overall prevalence of HAI was 5.4% in all patients present on a single day in two tertiary hospitals in
Table II Prevalence of hospital-acquired infection (HAI) according to exposure to intrinsic and extrinsic factors (result of multivariable analysis of association) in patients surveyed in two tertiary hospitals in Ulaanbaatar, Mongolia, 2008 Factorsa
Model Ib OR (95% CI)
(A) Intrinsic factors Age (years) <1 1–18 19–59 60 Admission mode Planned Emergency Admission source Home Other department or hospital Born in hospital Premature birth No Yes
Model IIc P
OR (95% CI)
Model IIId P
OR (95% CI)
1 0.3 (0.1–0.9) 0.5 (0.2–1.2) 0.5 (0.1–1.5)
0.032 0.142 0.208
1 1.8 (0.9–3.4)
0.058
1 3.2 (1.7–6.0) 0.4 (0.1–1.7)
<0.001 0.216
1 2.4 (1.1–5.4) 0.1 (0.0–1.4)
0.033 0.091
0.004
1 2.5 (0.8–8.2)
0.118
1 4.2 (1.6–10.8)
(B) Extrinsic factors Admitted hospital Hospital A Hospital B Length of hospital stay <3 days 3–7 days 8–14 days >14 days Surgical and other invasive procedures No Yes Peripheral intravascular catheter No Yes Urinary catheter No Yes Other catheters No Yes No. of catheter-days No catheter 1–2 3–4 5–7 >7 OR, odds ratio; CI, confidence interval. a Risk factors with P < 0.2 in the multivariable analysis. b OR of being infected with HAI mutually adjusted for all intrinsic variables in first column. c OR of being infected with HAI mutually adjusted for all extrinsic variables in first column. d OR of being infected with HAI mutually adjusted for all variables in first column.
1 0.3 (0.1–0.8) 0.7 (0.2–2.3) 0.8 (0.1–5.0)
P
– –
0.024 0.543 0.840 – –
1 2.7 (1.2–6.0)
0.017
1 4.6 (1.5–14.0)
0.007
1 2.0 (0.8–4.9) 3.3 (1.2–8.7) 4.6 (1.5–14.4)
0.123 0.018 0.010
1 2.2 (0.8–5.7) 3.6 (1.2–10.7) 5.1 (1.4–18.7)
0.112 0.019 0.014
1 2.9 (1.4–5.8)
0.004
1 2.8 (1.2–6.3)
0.013
1 6.6 (2.8–15.6)
<0.001
– –
– –
<0.001
1 9.5 (2.5–37.4)
0.001
1 8.6 (2.9–25.9)
<0.001
1 9.2 (1.3–63.6)
0.025
– – – – –
– – – – –
1 2.1 1.0 0.6 3.0
0.242 0.991 0.573 0.093
1 10.8 (3.9–9.0)
(0.6–7.0) (0.2–4.0) (0.1–3.1) (0.8–11.2)
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Table III Hospital-acquired infection (HAI) rates in selected countries (results of point prevalence studies) Countrya
Mauritius14 Slovenia15 Australia12 Indonesia16 Lebanon17 Hong Kong18 Lithuania19 Spain10 New Zealand13 Morocco20 Tunisia21 Malaysia22 Mongolia (current)
Year
1992 2001 1984 2006 1997 1980 1994 1990 1997 2005 2002 2001 2008
Hospital
4 19 269 2 14 1 1 123 1 1 1 1 2
HAI rates BSIb
UTIb
0.3 0.3 0.1 1.3 2.1 0.2 0.2 1.0 1.5 0.9 0.7 6.5 0.3
0.8 1.2 1.4 1.0 1.5 2.9 0.4 2.8 2.0 6.2 3.6 3.5 1.3
SSIb,c
RTIb
Othersb
1.8/8.2 0.7/4.4 2.2/4.6 1.5/6.3 2.4/5.0 2.1/7.6 1.4/8.4 2.2/5.9 2.9/9.0 5.8/21.5 5.0/10.0 3.7/12.9 1.1/3.9
0.5 1.0 1.2 – 2.5 2.8 4.5 1.5 2.7 2.9 6.4 4.3 1.3
1.5 1.8 1.4 3.3 – 0.9 2.7 2.4 4.7 2.0 2.1 1.1 1.4
Overall rateb
Culture test done
Antibiotics prescribed
4.9 5.0 6.3 7.1 8.5 8.9 9.2 9.9 13.8 17.8 17.9 19.1 5.4
– 35% – 5% 3.4% – 41% 61% 72% 32% 28% 68% 18.9%
34.5% – – 55% – 24% 26% 33% – 20% 46.8% 44% 59.8%
BSI, bloodstream infection; UTI, urinary tract infection; SSI, surgical site infection; RTI, respiratory tract infection. a Countries placed according to overall HAI rate. b Number of nosocomial infections per 100 admissions. c Number of SSIs per 100 patients undergoing surgery.
Ulaanbaatar, Mongolia. This is substantially higher than previous reports of 0.01–0.05% and suggests that official statistics grossly underestimate the burden of HAI in Mongolia.6,7 Among patients who underwent surgery, 3.9% had SSIs, whereas overall, 1.3–1.4% of patients had UTI, RTI and other infections and 0.3% had BSI. Compared to reports of HAI point prevalence in other selected countries that used US CDC definitions (Table III), our overall prevalence estimate is similar to that reported from Mauritius, Slovenia and Australia.12,14,15,24,25 Our prevalence estimate is slightly less than reported from Indonesia, Lebanon, Hong Kong, Lithuania and Spain, and substantially lower than reported from New Zealand, Morocco, Tunisia and Malaysia.10,13,16–22 Despite basic similarities in these studies it remains difficult to compare results due to many sources of variation, including methods of variable categorisation, risk factors studied, hospital services provided and differences in patient populations. Although closer to internationally reported prevalence values than the HRISRU reports, our overall prevalence of HAI of 5.4% was still lower than what might be expected given Mongolia’s status as a country in transitional stages of development. The prevalence of SSI was particularly low in hospital A, which was the main contributor to the lower than expected prevalence of HAI in the overall study. Surgical teams from the USA, Switzerland, Korea and other countries have been implementing joint programmes for last 5–10 years in hospital A and some advanced technologies have been introduced, including laparoscopy, new hand rubs, wound care antiseptic solutions and antibiotic-impregnated wound dressing materials. Low bed occupancy might also contribute. However, we also acknowledge that the lower than expected rate might be due to low sensitivity of diagnosis via our patient examinations. Whereas we endeavoured to maximise sensitivity of diagnosis via extensive training of ICPs and piloting of the study, it is possible that some cases of HAI were missed. We plan to undertake a future in-depth study of SSI prevalence in hospital A to identify reasons for the lower than expected prevalence. The level of antibiotic use found in our study is higher than that reported from all the comparable studies from other countries that we identified (Table III). In our study, hospitals used single antibiotics or combinations of simple antibiotics such as ampicillin and gentamicin for 1–5 days and, if there were no clinical improvements, treatment was reinforced with cephalosporins (cefotaxime, ceftriaxone and cefazolin) and metronidazole. Given the low prevalence of HAI we assume that this strategy of antibiotic prescribing is working well in the study hospitals.
Monitoring of antibiotic resistance is at a very early stage in Mongolia. S. aureus isolates are not investigated for meticillin resistance and, generally speaking, cultures are only taken when empiric antibiotic prescriptions fail. Diagnosis of HAI is limited by hospital laboratory capacity in Mongolia, which is low due to severe budget restrictions. It was notable that many HAI cases were diagnosed using the criteria ‘Physician’s diagnosis’ or ‘Physician institutes appropriate antimicrobial therapy’ rather than using laboratory criteria.24,25 Culture test results were available for only 18.9% of patients, which is higher than similar studies conducted in Indonesia and Lebanon but less than other, similar studies conducted in Slovenia, Lithuania, Morocco and Tunisia, and far below that of studies conducted in industrialised countries such as Spain, New Zealand and Malaysia, where culture test results were available for 70–80% of patients (Table III).10,13,15–17,19–22 Our multivariable logistic regression models revealed 11 HAI risk factors. Many of these have been found to be risk factors in other studies, including patient age, hospital, length of hospital stay, surgical and other invasive procedures and use of catheters.10,15–17,20,21 Although we acknowledge the limitations of the point prevalence study design, we present the first estimate of the prevalence of HAI in Mongolian hospitals derived from a systematic, prospective survey. The results suggest that the prevalence of HAI is much higher than previously reported, but still lower than in other developing or transition-economy nations. Acknowledgements We thank colleagues from the Ministry of Health, Mongolia, and the directors of three hospitals who facilitated our study. We are indebted to the following ICPs and members of the Mongolian Association of Infection Control Professionals who conducted the study: Drs Ts. Narangarav, G. Narantuya, Erdenetsetseg, S. Ouyngerel, Ts. Uyanga, R. Siez, B. Bayankhutag, B. Myadagmaa, B. Otgonchimeg, E. Gereltsetseg, E. Ononchimeg, I. Munkhjargal, G. Terbish, Ch. Munkhchimeg, D. Odsuren, M. Uranchimeg, and M. Narantuya. Many thanks to colleagues from the Center for Healthcare Related Infection Surveillance and Prevention, Queensland, Australia, especially J. Stackelroth, who provided guidance in the study design and in interpreting some of the results. Conflict of interest statement None declared.
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Funding sources Dr B.-E. Ider was supported by an Australian Leadership Award Scholarship Program, and the study was partly funded by the University of Queensland, School of Population Health.
References 1. Bolormaa T, Natsagdorj Ts, Tumurbat B, et al. Mongolia: health system review. Health Syst Transition 2007;9:87–93. 2. Government of Mongolia. Government resolution no. 129: approval of the National Programme for Control of Communicable Diseases. Ulaanbaatar: Government of Mongolia; 2002 [in Mongolian]. 3. Ministry of Health of Mongolia. Health sector strategic master plan, 2006–2015. Ulaanbaatar: Ministry of Health; 2005 [in Mongolian]. 4. World Bank. Mongolian health system at a crossroad: the incomplete transition to a post-Semashko model. Washington, DC: East Asian and Pacific Human Development; 2006. pp. 57–61. 5. Ministry of Health of Mongolia. Ministerial order No. 336: Strengthening prevention and control of hospital acquired infection. Ulaanbaatar: Ministry of Health; 1997 [in Mongolian]. 6. National Centre for Communicable Diseases. Health related infection surveillance and prevention unit’s annual report, 2004. Ulaanbaatar: NCCD; 2005. pp. 1–3. [in Mongolian]. 7. National Centre for Communicable Diseases. Health related infection surveillance and prevention unit’s annual report, 2008. Ulaanbaatar: NCCD; 2009. pp. 2–7. [in Mongolian]. 8. Ruden H, Gastmeier P, Daschner FD, Schumacher M. Nosocomial and community-acquired infections in Germany: summary of the results of the First National Prevalence Study (NIDEP). Infection 1997;25:199–202. 9. Emmerson AM, Enstone JE, Griffin M, Kelsey MC, Smyth ETM. The second national prevalence survey of infection in hospitals: overview of the results. J Hosp Infect 1996;32:175–190. 10. EPINE Working Group. Prevalence of hospital-acquired infections in Spain. J Hosp Infect 1992;20:1–13. 11. Liziolia A, Privitera G, Alliata E, et al. Prevalence of nosocomial infections in Italy: result from the Lombardy survey in 2000. J Hosp Infect 2003;54: 141–148.
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12. McLaws ML, Gold J, King K, Irwig LM, Berry G. The prevalence of nosocomial and community-acquired infections in Australian hospitals. Med J Aust 1988;149:582–590. 13. Nicholls TM, Morris AJ. Nosocomial infection in Auckland Healthcare hospitals. NZ Med J 1997;110:314–316. 14. Jepsen OB, Jensen LP, Zimakoff J, et al. Prevalence of infections and use of antibiotics among hospitalized patients in Mauritius: a nationwide survey for the planning of a national infection control programme. J Hosp Infect 1993;25:271–278. 15. Klavs I, Bufon Luznik T, Skerl M, et al. Prevalence of and risk factors for hospitalacquired infections in Slovenia: results of the first national survey, 2001. J Hosp Infect 2003;54:149–157. 16. Duerink DO, Roeshadi D, Wahjono H, et al. Surveillance of healthcare-associated infections in Indonesian hospitals. J Hosp Infect 2006;62:219–229. 17. Azzam R, Dramaix M. A one-day prevalence survey of hospital-acquired infections in Lebanon. J Hosp Infect 2001;49:74–78. 18. French GL, Cheng A, Farrington M. Prevalence survey of infection in a Hong Kong hospital using a standard protocol and microcomputer data analysis. J Hosp Infect 1987;9:132–142. 19. Valinteliene R, Jurkuvenas V, Jepsen OB. Prevalence of hospital-acquired infection in a Lithuanian hospital. J Hosp Infect 1996;34:321–329. 20. Jroundi I, Khoudri I, Azzouzi A, et al. Prevalence of hospital-acquired infection in a Moroccan university hospital. Am J Infect Control 2007;35: 412–416. 21. Kallel H, Bahoul M, Ksibi H, et al. Prevalence of hospital-acquired infection in a Tunisian hospital. J Hosp Infect 2005;59:343–347. 22. Hughes AJ, Ariffin N, Huat TL, et al. Prevalence of nosocomial infection and antibiotic use at a University Medical Center in Malaysia. Infect Control Hosp Epidemiol 2005;26:100–104. 23. Sanou J, Traore SS, Lankoande J, Ouedraogo RM, Sanou A. Survey of nosocomial infection prevalence in the surgery department of the Central National Hospital of Ouagadougou. Dakar Med 1999;44:105–108. 24. Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC definitions for nosocomial infections, 1988. Am J Infect Control 1988;16:128–140. 25. Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 2008;36:309–332. 26. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for prevention of surgical site infection, 1999. Am J Infect Control 1999;27: 97–132.
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Journal of Hospital Infection journal homepage: www.elsevierhealth.com/journals/jhin
Prevalence of hospital-acquired infections and antibiotic use in two tertiary Mongolian hospitals B.-E. Ider a, *, A. Clements a, b, J. Adams a, M. Whitby c, T. Muugolog d, e a
University of Queensland, School of Population Health, Brisbane, Queensland, Australia Australian Centre for International and Tropical Health, Queensland Institute of Medical Research, Brisbane, Queensland, Australia c Infection Management Services, Princess Alexandra Hospital, Brisbane, Queensland, Australia d Hospital Related Infection Surveillance and Research Unit, National Center for Communicable Diseases, Ulaanbaatar, Mongolia e Mongolian Association of Infection Control Professionals, Ulaanbaatar, Mongolia b
a r t i c l e i n f o
s u m m a r y
Article history: Received 24 August 2009 Accepted 13 January 2010 Available online 1 April 2010
Health statistics of Mongolia indicate that hospital-acquired infections (HAIs) occur in 0.01–0.05% of all hospital admissions. This is considerably lower than internationally reported rates. A one-day survey was conducted in two tertiary hospitals of Ulaanbaatar in September 2008 to estimate HAI prevalence, associated risk factors and patterns of antibiotic usage. Among 933 patients surveyed, 50 (5.4%) were diagnosed with HAI. Prevalence of surgical site infection was 1.1% (3.9% among surgical patients), bloodstream infection 0.3%, respiratory tract infection 1.3%, urinary tract infection 1.3%, and other HAI 1.4%. Microbiological investigations were only documented for 18.9% of all patients. A total of 558 patients (59.8%) were taking 902 courses of antibiotics; 92.1% of patients were prescribed antibiotics without a sensitivity test. Multiple logistic regression analysis revealed that HAI was significantly associated with the admission source, the hospital, length of hospital stay, surgical and other invasive procedures, urinary catheters and other indwelling devices. The study results were comparable with reports from some other developing countries and confirm that official statistics underestimate the true frequency of HAI in Mongolia. Ó 2010 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved.
Keywords: Hospital-acquired infection Mongolia Point prevalence study Prevalence Risk factors Under-reporting
Introduction As a consequence of the rapid political and structural changes that occurred in Mongolia in the early 1990s, the strong Sanitary Epidemiological Service that had been inherited from the socialist government was dismantled without replacement.1 Plans were adopted by the new, democratically elected government to reorganise the public health system, and these included a strategy for hospital infection control.2,3 However, implementation has been slow for a myriad of reasons, including resource limitations and a lack of expert personnel.4 A Hospital Related Infection Surveillance and Research Unit (HRISRU) has been established at the National Centre for Communicable Diseases (NCCD) in the capital city, Ulaanbaatar.5 The HRISRU has been collecting hospital-acquired infection (HAI)
* Corresponding author. Address: University of Queensland, School of Population Health, Australia. Tel.: þ61 73346 4829; fax: þ61 73365 5442. E-mail address: [email protected] (B.-E. Ider).
surveillance data since 1998 from all tertiary and secondary level hospitals. The reported prevalence of HAI has been 0.01–0.05% of all hospital admissions, with the highest prevalence (0.05%) reported for tertiary hospitals in Ulaanbaatar.6,7 Other than the HRISRU reports, there have been no published HAI prevalence studies from Mongolia. Meanwhile, other studies have shown that HAI prevalence varies from 3.5% to 13.8% in high income industrialised countries, and from 4.9% to 22.4% in middle and low income countries.8–23 The low observed rate of HAI in the HRSIRU reports is almost certainly due to considerable under-reporting. There are many potential reasons for under-reporting which are not the focus of this study. Accurate data on the burden of HAI are essential for resource planning and the formulation of policies and guidelines for infection control and surveillance. To address this need, we aimed to determine the first accurate estimate of overall HAI prevalence, as well as prevalence of internationally recognised types of HAI, in two tertiary hospitals of Ulaanbaatar. We also aimed to identify risk factors for HAI among patients in those hospitals, to provide evidence for future HAI control programmes.
0195-6701/$ – see front matter Ó 2010 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2010.01.016
B.-E. Ider et al. / Journal of Hospital Infection 75 (2010) 214–219
Methods Setting The two largest tertiary teaching hospitals in Ulaanbaatar as defined by service features and bed capacity, hereafter referred to as hospitals A and B, were chosen for the study. Hospital A has 544 beds and a bed occupancy of 75.7%. It has 14 departments (six surgical, seven medical and one intensive care/emergency unit), providing care for adults only. Hospital B has 733 beds with a bed occupancy of 71.9% and has 25 departments (six surgical, 12 medical, seven intensive care/emergency units). It delivers tertiary medical services to paediatric, obstetric and gynaecology patients. Ethical considerations and study population Ethical approval for the study was obtained from the National Medical Research Ethics Committee of Mongolia and the Medical Research Ethics Committee of the University of Queensland, Australia. All 940 inpatients in the hospitals on the study day, or a legal proxy, were asked to provide consent to participation and only seven patients (0.7%) refused. Definitions The current infection control guidelines in Mongolia lack standardised definitions for HAI. Therefore the US Centres for Disease Control and Prevention (CDC) definitions of HAI, widely utilised in similar studies, were used in the study for standardisation and comparison purposes.8,10,11,15–17,20–22,24,25 These categorise 41 diagnostic groups which were classified as: (1) surgical site infection (SSI), (2) bloodstream infection (BSI), (3) urinary tract infection (UTI), (4) respiratory tract infection (RTI) and (5) other infection. All infections with onset >48 h after admission were recorded as HAI. SSI in surgical patients who were readmitted due to infection within one month of surgery or within one year after an implant was placed, were also classified as HAI. Surgical patients with a clean or clean-contaminated wound class and who had symptoms of infection were recorded as having HAI.26 Patients with a contaminated or dirty-infected wound class were classified as having a community-acquired infection (CAI) together with all other infections. Antibiotic therapy was defined as prophylactic when it was prescribed to patients who had no progressive infections, including infectious comorbidities. Pilot study A pilot study was conducted in one general hospital of Ulaanbaatar to test and refine the survey methods. Eighteen infection control practitioners (ICPs) were recruited from tertiary and secondary level hospitals of Ulaanbaatar and the HRISRU for the pilot study. Data collection A one-day prevalence study was conducted during two consecutive weeks: the weeks starting 30 September 2008 in hospital A and 8 October 2008 in hospital B. On the study day, each of the 18 ICPs was designated 20–30 patients in surgical departments, intensive care and emergency units (IC&EU) or 30–40 patients in obstetrics and gynaecology (O&G), and medical departments. Data were recorded from each patient’s records, ward’s laboratory results and nursing books. Data included: hospital and department name, date of birth, gender, admission date and time, admission purpose (diagnostic or treatment), admission mode
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(emergency or planned), admission source (home, other hospital/ department, or born in hospital), admission diagnosis, comorbidities (premature birth, diabetes, chronic respiratory and cardiovascular diseases, immunocompromise (including chemotherapy, hormone or radiation therapy, acquired immune deficiency syndrome), antibiotic usage (name, duration and purpose), microbiological tests (sites, isolates and antimicrobial susceptibility), body temperature, laboratory results (leukocyte count, erythrocyte sedimentation rate, C-reactive protein and urine sediment) and radiography results. Presence of indwelling devices during the current hospital stay was recorded. The devices were categorised as: mechanical ventilation devices, central and peripheral venous catheters, urinary catheters, wound drains and other devices (including epidural catheters and nasogastric tubes). All surgical procedures and operations undergone during the previous 30 days and surgical prostheses placed during the previous 12 months were also noted. After transferring data to the data collection forms, the ICPs visited the wards to conduct patient examinations, where they determined whether patients belonged to one of three groups: patients with no infection, patients with HAI and patients with CAI. At the bedside, ICPs asked patients if they were experiencing specific clinical symptoms of infection (e.g. fever, shivering, chills or malaise). Patients were also asked to show the ICP any surgical wounds and catheter sites. Occurrence of HAI or CAI, as defined above, was recorded. Statistical analysis The statistical software packages SPSS 15.0 (SPSS Inc, Chicago, IL, USA) and STATA-10 (Stata Corp LP, College Station, TX, USA) were used in the analysis. Initial descriptive summary statistics were calculated. The CAI data were not analysed further, but a subsequent analysis was conducted to determine risk factors for HAI, with the patients from both hospitals grouped together. Explanatory variables were divided into those that were intrinsic and extrinsic to the patient. Bivariable analyses were performed using cross-tabulation and logistic regression methods. Odds ratio (OR), 95% confidence interval (95% CI) and P-value were estimated for each intrinsic and extrinsic variable. Explanatory variables with P < 0.2 were considered as candidates for subsequent multivariable models. The candidate variables were tested for multicolinearity and variables found to be colinear with other variables (as defined by a variance inflation factor >10) were removed. Backward stepwise logistic regression models were run for intrinsic (model I), extrinsic (model II) and both intrinsic and extrinsic (model III) groups of explanatory variables using an exit criterion of P > 0.2 and an entry criterion of P 0.1. Results Patient features Of the 933 surveyed patients, 423 (45.3%) were men and 510 (54.7%) were women. The mean age was 26.5 years (SD: 22.1; range: 0–93); 45.2 years in hospital A (N ¼ 405) and 12.2 years in hospital B (N ¼ 528). The mean length of stay from admission to study day was 5.7 days (range: 0–76; median: 5). Of these, 299 were surgical, 398 were medical, 160 were O&G and 76 were IC&EU patients. A total of 138 patients (14.8%) had a total of 275 indwelling devices. Peripheral venous catheters were the most common (142) followed by epidural catheters and nasogastric tubes (46), wound drains (41), urinary catheters (32), central venous catheters (9) and endotracheal tubes (5). Device utility levels were similar in both
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hospitals (13.6% and 15.7% for hospitals A and B respectively). Seventy-six patients had one device, 39 had two, nine had three, and 14 had four or more devices. In total, 253 (27.1%) patients had undergone 273 surgical episodes; 239 patients had one operation, ten patients had two, two patients had three, and two patients had four. The most common wound class was clean-contaminated, 146 (53.5%) patients, followed by dirty-infected wounds, 55 (20.1%) patients. The surgical site class composition was similar in the two hospitals. Infections Of 933 patients, 343 (36.8%) had an infection during their hospital stay (Table I). Of these, 293 patients were diagnosed with CAI and 50 with HAI, providing a crude prevalence of 31.4% for CAI and 5.4% for HAI. No patients were diagnosed as having two or more HAIs. Among HAIs, the most common infections were skin and tissue infections (grouped as ‘others’) (1.4%), followed by respiratory tract (1.3%), urinary tract (1.3%), surgical site (1.1%) and bloodstream (0.3%) infections. Hospital A had 15 HAI cases with an overall prevalence of 3.7%, whereas hospital B had 35 HAI cases with an overall prevalence of 6.6%. The prevalence of SSI among surgical patients was 2.4% (3/126) for hospital A, 5.5% (7/127) for hospital B and 3.9% (10/253) overall. Approximately two-thirds of SSI were deep or organ space infections.
Table I Infection outcomes among patients surveyed in two tertiary hospitals in Ulaanbaatar, Mongolia, 2008 Main variables
Hospital A
Hospital B
Patients with infectionsa Community-acquired infection (CAI) Hospital-acquired infection (HAI) HAIs by departmentb Surgical Medical Obstetrics and gynaecology Intensive care and emergency Types of HAIa Surgical site infection Bloodstream infection Urinary tract infection Respiratory tract infection Others List of HAIsa Incisional surgical wound infection Deep surgical wound infection Laboratory-confirmed bloodstream infection Clinical sepsis Symptomatic urinary tract infection Pneumonia Bronchitis, tracheobronchitis, bronchiolitis, tracheitis, without evidence of pneumonia Meningitis or ventriculitis Gastroenteritis Intra-abdominal infection Conjunctivitis Upper respiratory tract infection (pharyngitis, laryngitis, epiglottitis) Joint or bursa infection Skin infection (other than incisional wound infection) Soft tissue infection Breast abscess or mastitis Omphalitis in newborn
123 (30.4) 108 (26.7) 15 (3.7)
220 (41.6) 185 (35.0) 35 (6.6)
343 (36.8) 293 (31.4) 50 (5.4)
9 (4.9) 4 (1.9) – 2 (40.0)
6 (5.3) 14 (7.7) 6 (3.8) 9 (12.7)
15 (5.0) 18 (4.5) 6 (3.8) 11 (14.5)
3 (0.7) – 8 (2.0) 4 (1.0) –
7 3 4 8 13
10 3 12 12 13
(1.3) (0.6) (0.8) (1.5) (2.5)
2 (0.5) 1 (0.2) –
1 (0.2) 6 (1.1) 1 (0.2)
– 8 (2.0) – 1 (0.2)
2 (0.4) 4 (0.8) 5 (0.9) –
– – – – 3 (0.7)
2 1 1 3 3
(0.4) (0.2) (0.2) (0.6) (0.6)
Total
(1.1) (0.3) (1.3) (1.3) (1.4)
3 (0.3) 7 (0.8) 1 (0.1) 2 12 5 1
(0.2) (1.3) (0.5) (0.1)
2 1 1 3 6
(0.2) (0.1) (0.1) (0.3) (0.6)
– –
1 (0.2) 1 (0.2)
1 (0.1) 1 (0.1)
– – –
1 (0.2) 1 (0.2) 2 (0.4)
1 (0.1) 1 (0.1) 2 (0.2)
Values in parentheses are percentages. a Denominator is the total number of patients. b Denominator is total number of patients in this group of departments.
Microbiological testing Of all patients, 176 (18.9%) had 233 (including seven missed) culture tests. Of these, 146 (83.0%) patients had one and the remaining 30 (17.0%) had repeated microbiological tests (up to six times) during their hospital stay. Cultures from the urine (50.4%), skin including eye, ear and vagina (16.4%), and surgical wound (11.5%) were the most common. Among 226 cultures, 137 (60.6%) yielded no pathogens and for 6 (2.7%) the results were pending at the time of the study, leaving 83 (36.7%) from which a pathogen had been isolated. The most common pathogens were Escherichia coli (31.3%) and Staphylococcus aureus (20.5%). In hospital A these pathogens were isolated from 33.3% and 36.4% of all cultures respectively. Among 50 patients diagnosed with HAI, 23 (46.0%) had documented microbiological results. Cultures were taken from urine (14), blood (8), swabs other than surgical wound (7), surgical wound (4), sterile fluids (3) and sputum (1). Isolated micro-organisms were E. coli (7), S. aureus (4), Enterobacter spp. (3), Enterococcus spp. (1), Proteus mirabilis (1), Candida spp. (1) and, in one case, an unidentified cocci on vaginal smear (1). Antibiotic use A total of 558 (59.8%) patients were taking 902 courses of antibiotics with the average number of antibiotics per patient being 1.62 (SD: 0.88; range: 1–6). In hospital A, 208 (51.4%) patients were taking 308 antibiotic courses with an average of 1.48 (SD: 0.75; range: 1–5) antibiotics per patient, whereas in hospital B, 350 (66.3%) patients were taking 594 courses with an average of 1.70 (SD: 0.94; range: 1–6) antibiotics per patient. At the time of the study, the mean duration of antibiotic therapy was 3.63 days (SD: 2.47; range: 0–14; median: 4.0) in hospital A, 3.71 days (SD: 3.21; range: 0–22; median: 3.0) in hospital B, and 3.68 days (SD: 2.90; range: 0–22; median: 3.0) overall. Twenty-two types of antibiotic were administered to patients, the most common being ampicillin, gentamicin and cefazolin, together accounting for 72.2% of all antibiotics administered. The most commonly prescribed antibiotics were a combination of ampicillin and gentamicin in hospital B and sole administration of cefazolin or ampicillin in hospital A. A total of 567 (64.9%) antibiotic courses were prescribed for treatment of infections. Ampicillin (27.0%), cefazolin (22.2%), gentamicin (20.6%), metronidazole (6.9%) and penicillin (4.2%) were the most frequently prescribed. The other 306 (35.1%) courses were prescribed for prophylactic purposes, mainly for surgical patients, patients with trauma or immunocompromised patients including cancer patients and preterm newborns. Ampicillin (40.5%), gentamicin (21.2%), cefazolin (15.0%), metronidazole (4.9%) and cefotaxime (3.9%) were the most commonly prescribed antibiotics for prophylaxis. Among 50 patients diagnosed with HAI, 47 (94.0%) were being administered antibiotics with an average number of antibiotics of 2.30 (SD: 1.19; range: 0–6) per patient. At the time of the study, the mean duration of antibiotic treatment was 5.74 days (SD: 4.51, range: 0–22; median: 5.0). These patients received a total of 107 antibiotic courses, with the most common being gentamicin (22), ampicillin (21), cefazolin (19), metronidazole (12) and cefotaxime (10). As elsewhere in Mongolia, the manual disc diffusion method is the only method of antibiotic susceptibility testing in these two hospitals. Commercially available discs for 12–15 commonly prescribed antibiotics are used. Fifty-one (5.5%) patients had a total of 70 antibiotic sensitivity tests conducted on bacterial isolates during their hospital stay, which represents 7.9% of those patients being administered antibiotics. The remaining 92.1% of patients were administered antibiotics without a sensitivity test being done, including 80.0% of patients diagnosed with HAI.
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For 70 tests conducted, sensitivity was assessed for 15 types of antibiotic. The antibiotics to which most pathogens were sensitive included cefotaxime (47.1%), ciprofloxacin (21.4%), ceftriaxone (15.7%), gentamicin (15.7%) and cefazolin (14.3%). In hospital A, the antibiotics to which most pathogens were sensitive were cefotaxime (68.7%) and ciprofloxacin (40.6%); in hospital B, they were cefotaxime (29.0%) and cefazolin (23.7%). HAI risk factors Among intrinsic factors, the patient’s age, admission mode, admission source, premature birth and presence of other allied conditions were found to be significantly associated with HAI in the bivariable analysis. Among extrinsic factors, hospital, department, patient’s length of hospital stay, surgical and other invasive procedures, indwelling device (mechanical ventilation, central and peripheral intravascular cannulas, urinary and other catheters) and
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number and duration of indwelling devices were significantly associated with HAIs in the bivariable analysis. In the multivariable model with intrinsic risk factors, only four variables had P < 0.2: patient age, admission mode, admission source, and premature birth (Table II). In the model with extrinsic factors, six variables had P < 0.2: hospital, length of hospital stay, surgical and other invasive procedures, use of peripheral intravascular, urinary catheters and other indwelling devices. In the overall model, with both intrinsic and extrinsic factors, six factors were significant: admission source, hospital, length of hospital stay, surgical and other invasive procedures, urinary catheters and other indwelling devices (i.e. epidural catheters and nasogastric tubes). Discussion We found that the overall prevalence of HAI was 5.4% in all patients present on a single day in two tertiary hospitals in
Table II Prevalence of hospital-acquired infection (HAI) according to exposure to intrinsic and extrinsic factors (result of multivariable analysis of association) in patients surveyed in two tertiary hospitals in Ulaanbaatar, Mongolia, 2008 Factorsa
Model Ib OR (95% CI)
(A) Intrinsic factors Age (years) <1 1–18 19–59 60 Admission mode Planned Emergency Admission source Home Other department or hospital Born in hospital Premature birth No Yes
Model IIc P
OR (95% CI)
Model IIId P
OR (95% CI)
1 0.3 (0.1–0.9) 0.5 (0.2–1.2) 0.5 (0.1–1.5)
0.032 0.142 0.208
1 1.8 (0.9–3.4)
0.058
1 3.2 (1.7–6.0) 0.4 (0.1–1.7)
<0.001 0.216
1 2.4 (1.1–5.4) 0.1 (0.0–1.4)
0.033 0.091
0.004
1 2.5 (0.8–8.2)
0.118
1 4.2 (1.6–10.8)
(B) Extrinsic factors Admitted hospital Hospital A Hospital B Length of hospital stay <3 days 3–7 days 8–14 days >14 days Surgical and other invasive procedures No Yes Peripheral intravascular catheter No Yes Urinary catheter No Yes Other catheters No Yes No. of catheter-days No catheter 1–2 3–4 5–7 >7 OR, odds ratio; CI, confidence interval. a Risk factors with P < 0.2 in the multivariable analysis. b OR of being infected with HAI mutually adjusted for all intrinsic variables in first column. c OR of being infected with HAI mutually adjusted for all extrinsic variables in first column. d OR of being infected with HAI mutually adjusted for all variables in first column.
1 0.3 (0.1–0.8) 0.7 (0.2–2.3) 0.8 (0.1–5.0)
P
– –
0.024 0.543 0.840 – –
1 2.7 (1.2–6.0)
0.017
1 4.6 (1.5–14.0)
0.007
1 2.0 (0.8–4.9) 3.3 (1.2–8.7) 4.6 (1.5–14.4)
0.123 0.018 0.010
1 2.2 (0.8–5.7) 3.6 (1.2–10.7) 5.1 (1.4–18.7)
0.112 0.019 0.014
1 2.9 (1.4–5.8)
0.004
1 2.8 (1.2–6.3)
0.013
1 6.6 (2.8–15.6)
<0.001
– –
– –
<0.001
1 9.5 (2.5–37.4)
0.001
1 8.6 (2.9–25.9)
<0.001
1 9.2 (1.3–63.6)
0.025
– – – – –
– – – – –
1 2.1 1.0 0.6 3.0
0.242 0.991 0.573 0.093
1 10.8 (3.9–9.0)
(0.6–7.0) (0.2–4.0) (0.1–3.1) (0.8–11.2)
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Table III Hospital-acquired infection (HAI) rates in selected countries (results of point prevalence studies) Countrya
Mauritius14 Slovenia15 Australia12 Indonesia16 Lebanon17 Hong Kong18 Lithuania19 Spain10 New Zealand13 Morocco20 Tunisia21 Malaysia22 Mongolia (current)
Year
1992 2001 1984 2006 1997 1980 1994 1990 1997 2005 2002 2001 2008
Hospital
4 19 269 2 14 1 1 123 1 1 1 1 2
HAI rates BSIb
UTIb
0.3 0.3 0.1 1.3 2.1 0.2 0.2 1.0 1.5 0.9 0.7 6.5 0.3
0.8 1.2 1.4 1.0 1.5 2.9 0.4 2.8 2.0 6.2 3.6 3.5 1.3
SSIb,c
RTIb
Othersb
1.8/8.2 0.7/4.4 2.2/4.6 1.5/6.3 2.4/5.0 2.1/7.6 1.4/8.4 2.2/5.9 2.9/9.0 5.8/21.5 5.0/10.0 3.7/12.9 1.1/3.9
0.5 1.0 1.2 – 2.5 2.8 4.5 1.5 2.7 2.9 6.4 4.3 1.3
1.5 1.8 1.4 3.3 – 0.9 2.7 2.4 4.7 2.0 2.1 1.1 1.4
Overall rateb
Culture test done
Antibiotics prescribed
4.9 5.0 6.3 7.1 8.5 8.9 9.2 9.9 13.8 17.8 17.9 19.1 5.4
– 35% – 5% 3.4% – 41% 61% 72% 32% 28% 68% 18.9%
34.5% – – 55% – 24% 26% 33% – 20% 46.8% 44% 59.8%
BSI, bloodstream infection; UTI, urinary tract infection; SSI, surgical site infection; RTI, respiratory tract infection. a Countries placed according to overall HAI rate. b Number of nosocomial infections per 100 admissions. c Number of SSIs per 100 patients undergoing surgery.
Ulaanbaatar, Mongolia. This is substantially higher than previous reports of 0.01–0.05% and suggests that official statistics grossly underestimate the burden of HAI in Mongolia.6,7 Among patients who underwent surgery, 3.9% had SSIs, whereas overall, 1.3–1.4% of patients had UTI, RTI and other infections and 0.3% had BSI. Compared to reports of HAI point prevalence in other selected countries that used US CDC definitions (Table III), our overall prevalence estimate is similar to that reported from Mauritius, Slovenia and Australia.12,14,15,24,25 Our prevalence estimate is slightly less than reported from Indonesia, Lebanon, Hong Kong, Lithuania and Spain, and substantially lower than reported from New Zealand, Morocco, Tunisia and Malaysia.10,13,16–22 Despite basic similarities in these studies it remains difficult to compare results due to many sources of variation, including methods of variable categorisation, risk factors studied, hospital services provided and differences in patient populations. Although closer to internationally reported prevalence values than the HRISRU reports, our overall prevalence of HAI of 5.4% was still lower than what might be expected given Mongolia’s status as a country in transitional stages of development. The prevalence of SSI was particularly low in hospital A, which was the main contributor to the lower than expected prevalence of HAI in the overall study. Surgical teams from the USA, Switzerland, Korea and other countries have been implementing joint programmes for last 5–10 years in hospital A and some advanced technologies have been introduced, including laparoscopy, new hand rubs, wound care antiseptic solutions and antibiotic-impregnated wound dressing materials. Low bed occupancy might also contribute. However, we also acknowledge that the lower than expected rate might be due to low sensitivity of diagnosis via our patient examinations. Whereas we endeavoured to maximise sensitivity of diagnosis via extensive training of ICPs and piloting of the study, it is possible that some cases of HAI were missed. We plan to undertake a future in-depth study of SSI prevalence in hospital A to identify reasons for the lower than expected prevalence. The level of antibiotic use found in our study is higher than that reported from all the comparable studies from other countries that we identified (Table III). In our study, hospitals used single antibiotics or combinations of simple antibiotics such as ampicillin and gentamicin for 1–5 days and, if there were no clinical improvements, treatment was reinforced with cephalosporins (cefotaxime, ceftriaxone and cefazolin) and metronidazole. Given the low prevalence of HAI we assume that this strategy of antibiotic prescribing is working well in the study hospitals.
Monitoring of antibiotic resistance is at a very early stage in Mongolia. S. aureus isolates are not investigated for meticillin resistance and, generally speaking, cultures are only taken when empiric antibiotic prescriptions fail. Diagnosis of HAI is limited by hospital laboratory capacity in Mongolia, which is low due to severe budget restrictions. It was notable that many HAI cases were diagnosed using the criteria ‘Physician’s diagnosis’ or ‘Physician institutes appropriate antimicrobial therapy’ rather than using laboratory criteria.24,25 Culture test results were available for only 18.9% of patients, which is higher than similar studies conducted in Indonesia and Lebanon but less than other, similar studies conducted in Slovenia, Lithuania, Morocco and Tunisia, and far below that of studies conducted in industrialised countries such as Spain, New Zealand and Malaysia, where culture test results were available for 70–80% of patients (Table III).10,13,15–17,19–22 Our multivariable logistic regression models revealed 11 HAI risk factors. Many of these have been found to be risk factors in other studies, including patient age, hospital, length of hospital stay, surgical and other invasive procedures and use of catheters.10,15–17,20,21 Although we acknowledge the limitations of the point prevalence study design, we present the first estimate of the prevalence of HAI in Mongolian hospitals derived from a systematic, prospective survey. The results suggest that the prevalence of HAI is much higher than previously reported, but still lower than in other developing or transition-economy nations. Acknowledgements We thank colleagues from the Ministry of Health, Mongolia, and the directors of three hospitals who facilitated our study. We are indebted to the following ICPs and members of the Mongolian Association of Infection Control Professionals who conducted the study: Drs Ts. Narangarav, G. Narantuya, Erdenetsetseg, S. Ouyngerel, Ts. Uyanga, R. Siez, B. Bayankhutag, B. Myadagmaa, B. Otgonchimeg, E. Gereltsetseg, E. Ononchimeg, I. Munkhjargal, G. Terbish, Ch. Munkhchimeg, D. Odsuren, M. Uranchimeg, and M. Narantuya. Many thanks to colleagues from the Center for Healthcare Related Infection Surveillance and Prevention, Queensland, Australia, especially J. Stackelroth, who provided guidance in the study design and in interpreting some of the results. Conflict of interest statement None declared.
B.-E. Ider et al. / Journal of Hospital Infection 75 (2010) 214–219
Funding sources Dr B.-E. Ider was supported by an Australian Leadership Award Scholarship Program, and the study was partly funded by the University of Queensland, School of Population Health.
References 1. Bolormaa T, Natsagdorj Ts, Tumurbat B, et al. Mongolia: health system review. Health Syst Transition 2007;9:87–93. 2. Government of Mongolia. Government resolution no. 129: approval of the National Programme for Control of Communicable Diseases. Ulaanbaatar: Government of Mongolia; 2002 [in Mongolian]. 3. Ministry of Health of Mongolia. Health sector strategic master plan, 2006–2015. Ulaanbaatar: Ministry of Health; 2005 [in Mongolian]. 4. World Bank. Mongolian health system at a crossroad: the incomplete transition to a post-Semashko model. Washington, DC: East Asian and Pacific Human Development; 2006. pp. 57–61. 5. Ministry of Health of Mongolia. Ministerial order No. 336: Strengthening prevention and control of hospital acquired infection. Ulaanbaatar: Ministry of Health; 1997 [in Mongolian]. 6. National Centre for Communicable Diseases. Health related infection surveillance and prevention unit’s annual report, 2004. Ulaanbaatar: NCCD; 2005. pp. 1–3. [in Mongolian]. 7. National Centre for Communicable Diseases. Health related infection surveillance and prevention unit’s annual report, 2008. Ulaanbaatar: NCCD; 2009. pp. 2–7. [in Mongolian]. 8. Ruden H, Gastmeier P, Daschner FD, Schumacher M. Nosocomial and community-acquired infections in Germany: summary of the results of the First National Prevalence Study (NIDEP). Infection 1997;25:199–202. 9. Emmerson AM, Enstone JE, Griffin M, Kelsey MC, Smyth ETM. The second national prevalence survey of infection in hospitals: overview of the results. J Hosp Infect 1996;32:175–190. 10. EPINE Working Group. Prevalence of hospital-acquired infections in Spain. J Hosp Infect 1992;20:1–13. 11. Liziolia A, Privitera G, Alliata E, et al. Prevalence of nosocomial infections in Italy: result from the Lombardy survey in 2000. J Hosp Infect 2003;54: 141–148.
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12. McLaws ML, Gold J, King K, Irwig LM, Berry G. The prevalence of nosocomial and community-acquired infections in Australian hospitals. Med J Aust 1988;149:582–590. 13. Nicholls TM, Morris AJ. Nosocomial infection in Auckland Healthcare hospitals. NZ Med J 1997;110:314–316. 14. Jepsen OB, Jensen LP, Zimakoff J, et al. Prevalence of infections and use of antibiotics among hospitalized patients in Mauritius: a nationwide survey for the planning of a national infection control programme. J Hosp Infect 1993;25:271–278. 15. Klavs I, Bufon Luznik T, Skerl M, et al. Prevalence of and risk factors for hospitalacquired infections in Slovenia: results of the first national survey, 2001. J Hosp Infect 2003;54:149–157. 16. Duerink DO, Roeshadi D, Wahjono H, et al. Surveillance of healthcare-associated infections in Indonesian hospitals. J Hosp Infect 2006;62:219–229. 17. Azzam R, Dramaix M. A one-day prevalence survey of hospital-acquired infections in Lebanon. J Hosp Infect 2001;49:74–78. 18. French GL, Cheng A, Farrington M. Prevalence survey of infection in a Hong Kong hospital using a standard protocol and microcomputer data analysis. J Hosp Infect 1987;9:132–142. 19. Valinteliene R, Jurkuvenas V, Jepsen OB. Prevalence of hospital-acquired infection in a Lithuanian hospital. J Hosp Infect 1996;34:321–329. 20. Jroundi I, Khoudri I, Azzouzi A, et al. Prevalence of hospital-acquired infection in a Moroccan university hospital. Am J Infect Control 2007;35: 412–416. 21. Kallel H, Bahoul M, Ksibi H, et al. Prevalence of hospital-acquired infection in a Tunisian hospital. J Hosp Infect 2005;59:343–347. 22. Hughes AJ, Ariffin N, Huat TL, et al. Prevalence of nosocomial infection and antibiotic use at a University Medical Center in Malaysia. Infect Control Hosp Epidemiol 2005;26:100–104. 23. Sanou J, Traore SS, Lankoande J, Ouedraogo RM, Sanou A. Survey of nosocomial infection prevalence in the surgery department of the Central National Hospital of Ouagadougou. Dakar Med 1999;44:105–108. 24. Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC definitions for nosocomial infections, 1988. Am J Infect Control 1988;16:128–140. 25. Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 2008;36:309–332. 26. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for prevention of surgical site infection, 1999. Am J Infect Control 1999;27: 97–132.