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Rates of Hospital-Acquired Respiratory Illness in Bangladeshi Tertiary Care Hospitals: Results from a Low-Cost Pilot Surveillance Strategy

  1. Emily S. Gurley1,
  2. Rashid Uz Zaman1,
  3. Rebeca Sultana1,
  4. Michael Bell3,
  5. Alicia M. Fry3,
  6. Arjun Srinivasan3,
  7. Mahmudur Rahman2,
  8. M. Waliur Rahman1,
  9. M. Jahangir Hossain1, and
  10. Stephen P. Luby1,3
  1. 1International Centre for Diarrheal Diseases Research, Bangladesh (ICDDR,B)
  2. 2Institute for Epidemiology, Disease Control, and Research, Ministry of Health and Family Welfare, Government of Bangladesh, Dhaka, Bangladesh
  3. 3Centers for Disease Control and Prevention, Atlanta, Georgia
  1. Reprints or correspondence: Dr Emily S. Gurley, GPO 128, Mohakhali, Dhaka-1000, Bangladesh (egurley{at}icddrb.org).
 
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Abstract

Background. Patients hospitalized in resource-poor health care settings are at increased risk for hospital-acquired respiratory infections due to inadequate infrastructure.

Methods. From 1 April 2007 through 31 March 2008, we used a low-cost surveillance strategy to identify new onset of respiratory symptoms in patients hospitalized for >172 h and in health care workers in medicine and pediatric wards at 3 public tertiary care hospitals in Bangladesh.

Results. During 46,273 patient-days of observation, we recorded 136 episodes of hospital-acquired respiratory disease, representing 1.7% of all patient hospital admissions; rates by ward ranged from 0.8 to 15.8 cases per 1000 patient-days at risk. We identified 22 clusters of respiratory disease, 3 of which included both patients and health care workers. Of 226 of heath care workers who worked on our surveillance wards, 61 (27%) experienced a respiratory illness during the study period. The cost of surveillance was US$43 per month per ward plus 30 min per day in data collection.

Conclusions. Patients on these study wards frequently experienced hospital-acquired respiratory infections, including 1 in every 20 patients hospitalized for >72 h on 1 ward. The surveillance method was useful in calculating rates of hospital-acquired respiratory illness and could be used to enhance capacity to quickly detect outbreaks of respiratory disease in health care facilities where systems for outbreak detection are currently limited and to test interventions to reduce transmission of respiratory pathogens in resource-poor settings.

Hospital-acquired infections are a challenge for all health care facilities, particularly in resource-poor health care settings where inadequate access to running water and soap, patient crowding, and insufficient personnel and staff training may contribute to higher rates of infections. A large study conducted in 14 countries showed that, on average, 8.7% of patients had hospital-acquired infections but that the burden is higher in Southeast Asia, where 10% of patients developed such infections [1]. Recent data from lower-income countries suggest that 6.5%-33% of patients have hospital-acquired infections,

with pneumonia being among the most frequent [2–5]. Hospital-acquired infections result in higher mortality rates, higher costs, and increased length of hospital stays. The World Health Organization has declared preventing hospital-acquired infections in lower-income countries a global priority [6], although we have little evidence to suggest which interventions work best in these settings to prevent such infections.

There are few published reports about the burden of hospital-acquired infections in lower-income countries such as Bangladesh. These health care facilities frequently have insufficient resources for surveillance and infection control programs, creating a scenario where facilities with the highest risk of nosocomial infections are least likely to report them. In Bangladesh, hospital- acquired respiratory infections are of particular interest because of regional threats from emerging diseases, such as severe acute respiratory syndrome and Nipah virus, which have caused nosocomial outbreaks in the past decade [7–9]. The emergence of novel strains of influenza, such as pandemic H1N1 [10], warrant strengthening systems for detection and response to outbreaks of respiratory disease in health care facilities.

Hospital-acquired respiratory infections are preventable. Centers for Disease Control and Prevention (CDC) recommendations for protecting patients and health care workers in the workplace are based on standard and droplet precautions and assume sufficient laboratory infrastructure and resources for disposable personal protective equipment and vaccination [11]. Although international standards of infection control are often not feasible in resource-poor settings, these standards can be adapted to such settings [12], and lower-cost interventions, such as the promotion of hand hygiene, can have a substantial impact on reducing infections [13, 14]. However, uptake of even low-cost interventions in resource-poor settings are driven by cost-effectiveness estimates, which are in turn driven by burden of disease [2]. More regional and national data on the burden of hospital-acquired respiratory infections are needed to effectively promote investments in infection control programs and evaluate their success [12].

Given the risk posed by outbreaks of respiratory disease in regional hospitals, we aimed to pilot a surveillance strategy that might be used in this and similar settings. Traditional surveillance methods were not practical in this setting; local resources for specimen collection and laboratory diagnosis of specific pathogens were inadequate. Therefore, we piloted a surveillance strategy that used data already being collected as part of routine patient care. The primary objective was to determine whether our approach was successful at engaging hospitals to report data on hospital-acquired respiratory disease, including clusters of disease. The secondary objective was to estimate the burden of these infections in Bangladeshi hospitals to generate an evidence base for intervention.

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Methods

From 1 April 2007 through 31 March 2008, we conducted surveillance for hospital-acquired respiratory infections in patients hospitalized for >72 h in 1 adult male medicine ward and 1 pediatric medicine ward in each of 3 public tertiary care hospitals in Bangladesh. These hospitals had no critical care units, so patients with severe disease were hospitalized in these wards alongside other patients. Patients in these hospitals did not receive ventilatory support. Each ward consisted of 30–50 beds, and patients typically hospitalized in these wards had a wide variety of acute and chronic diseases. Hospitals were chosen on the basis of their previous research relationship with the International Centre for Diarrheal Disease Research, Bangladesh (ICDDR,B), and interest by hospital administrators in participating in the project.

One physician employed at each study ward was provided a small monthly stipend (∼US$43) for their participation in the study. Each morning, the surveillance physician would review patient medical records and clinical progression during rounds to identify patients hospitalized for >72 h who developed new onset of documented fever, cough, runny nose, difficult breathing, or diarrhea. When a patient who met these criteria was identified, the physician completed a structured form documenting the patient's age, sex, admitting diagnosis, date of admission, dates of new onset of symptoms, and date and outcome of hospitalization (ie, the patient was discharged, was referred, or died). After November 2007, physicians also recorded whether the patient received antibiotics within the first 72 h of hospitalization. Monthly summaries of the total numbers of patients admitted and the total number of patient-days in each ward were tallied. These duties required ∼30 min per ward per day.

A hospital-acquired respiratory infection was defined as new onset of cough, runny nose, or difficulty breathing (with or without fever or diarrhea) after 72 h of hospitalization. Standard guidelines from the CDC advocate for defining hospital-acquired infections as those that occur 48 h after hospitalization [15], but we chose to use 72 h to increase the specificity of our definition, as has been done in other studies in low-income countries [5, 16]. The proportion of patients with hospital- acquired respiratory infections and rates of these infections per 1000 patient-days at risk were calculated by ward and month. The mean number of days of hospitalization for patients with hospital-acquired respiratory infections was calculated.

In addition, we requested that health care workers on these wards report any new illnesses they experienced to the sur veillance physicians. We asked surveillance physicians to follow-up with health care workers every 2 weeks to inquire about illnesses experienced. For each illness identified, the date of onset, symptoms, and the profession of the health care worker were recorded. We counted the number of staff members working on each ward during November 2007 and used this estimate as the denominator to calculate the percentage of health care workers experiencing illnesses with respiratory symptoms during the study period.

We plotted the dates of onset of new respiratory symptoms for patients and staff by ward to look for clusters of disease. We defined a cluster of disease as ⩾3 patients or health care workers developing new onset of respiratory symptoms within 1 week of each other on the same ward.

Approximately once per month, research staff visited surveillance hospitals to inquire about surveillance activities and check data log books in an effort to promote quality in data collection. On receipt of the data forms each month, the ICDDR,B staff checked the forms for mathematical errors and completion. Because this was a pilot surveillance project, a study protocol was reviewed and approved by the ICDDR,B and CDC institutional review boards.

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Results

In the 6 wards under surveillance, 22,652 patients were admitted during the study year, and 8040 (36%) of those patients were hospitalized for >72 h (Table 1). On average, 11 patients were hospitalized for every 10 beds (Table 1). Patients sometimes shared beds or were cared for on mattresses on the floor. During 22,153 patient-days at risk, we recorded 136 episodes of hospital-acquired respiratory illness. These episodes represented 1.7% of all patients hospitalized for ∼72 h and occurred at a rate of 6.1 cases per 1000 patient-days. Our analysis identified 22 clusters of respiratory disease in these hospitals, ranging in size from 4 to 19 cases (Table 1). All but 4 clusters included patients and health care workers. Rates varied among the hospitals; hospital B's adult male medicine ward reported the highest rate at 15.8 cases per 1000 patient-days (Table 1). The mean length of hospital stay was 3.3 days overall and 8.3 days for patients with hospital-acquired respiratory illness (Table 1).

Table 1.
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Table 1.

Patient Observation Days, Bed Occupancy Rates, Rates of New Onset of Respiratory Symptoms, Patient Length of Stay, and Number of Disease Clusters Observed, by Hospital Ward, April 2007 to March 2008.

Fifty-six (41%) of 136 patients with hospital-acquired respiratory illness had new onset of both cough and fever, and 8 (6%) had new onset of fever, cough, and difficult breathing (Table 2). These patients represented all age groups. Of 136 patients with hospital-acquired respiratory illness, 126 (93%) were discharged from the hospital, 5 (4%) left against medical advice, and 3 (2%) died in the hospital. All 3 deaths occurred in the pediatric ward of hospital C during 3 weeks in November and December 2007; 2 deaths occurred in neonates with admitting diagnoses of prematurity and birth asphyxia, and the third occurred in a young child admitted with glomerular nephritis. All 3 experienced new onset of fever, cough, and difficult breathing after 3 days of hospitalization. Twenty-nine (21%) of 136 patients with new onset of respiratory symptoms were discharged from the hospital within a day of onset of symptoms, and, therefore, the outcome of their illness remains unknown; 9 (31%) of 29 of these patients experienced new onset of fever and cough, 8 (28%) experienced only runny nose, and 4 (14%) experienced difficult breathing. Among the 54 patients with new onset of respiratory symptoms identified after November 2007, 27 (50%) had received antibiotics within the first 72 h of hospitalization. Patients with new onset of respiratory symptoms commonly had admitting diagnoses of stroke, myocardial infarction, or other cardiovascular disease (34 [25%] of 136) and gastrointestinal or hepatic disease (21 [15%] of 136) (Table 2).

Table 2.
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Table 2.

Characteristics of Patients with Hospital-Acquired Respiratory Illness

Rates of hospital-acquired respiratory illness varied not only among wards and hospitals but also by month within wards (Figure 1). Eight clusters occurred in the pediatric wards in hospitals B and C during the cooler postmonsoon and winter months. Among adult male medicine wards, hospital B had the only ward to consistently report new respiratory infections and clusters of disease throughout the year (Figure 2).

Figure 1.
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Figure 1.

Rates of hospital-acquired respiratory illness per 1000 patient- days at risk and clusters of respiratory disease in pediatric medicine wards by month and hospital.

Figure 2.
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Figure 2.

Rates of hospital-acquired respiratory illness per 1000 patient- days at risk and clusters of respiratory disease in male medicine wards by month and hospital.

Approximately 226 heath care staff members worked on our surveillance wards, and among them 61 (27%) reported experiencing a respiratory illness during the study period. Thirty (75%) of 40 health care workers on the adult medicine ward of hospital B experienced respiratory illness compared with only 6%–24% of staff members on other wards (Table 3). Thirty (49%) of 61 health care workers who reported illnesses experienced both cough and fever. Forty-two (69%) of 61 illnesses occurred in physicians (Table 3). A cluster of 3 health care worker respiratory illnesses was reported during the same weeks as the deaths in the pediatric ward in hospital C. On average, each illness episode lasted 4.3 days, and health care staff worked 230 (89%) of the 260 days they were ill (Table 3).

Table 3.
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Table 3.

Characteristics of Health Care Workers Experiencing Respiratory Illnesses during the Study Period

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Discussion

Our surveillance pilot was successful at generating data on risk of hospital-acquired respiratory infections in Bangladeshi hospitals and identifying clusters of disease that may represent important public health events. On average, these infections occurred in 17 of every 1000 patients admitted for >72 h, which is similar to other published rates from less developed countries [5, 17]. The adult medicine ward of hospital B had clusters of respiratory disease identified almost monthly, and in pediatric wards, clusters appeared most frequently in the winter months. Three deaths were associated with 1 cluster, but patient out comes for many patients in clusters remain unknown because patients frequently leave the hospital with respiratory symptoms. Patients leaving these hospitals with respiratory infections may pose a health risk to others in their communities [18, 19]. The fact that 25% of hospital-acquired respiratory disease occurred in patients hospitalized for cardiovascular disease, stroke, and myocardial infarction is concerning, because acute respiratory illness in this group—particularly influenza—is associated with increased risk of complications and poor health outcomes [20–22].

The data were not analyzed on a monthly basis by hospital staff; however, rates could easily be calculated and clusters identified in hospitals in real time. Because this surveillance tool used existing hospital staff and resources, it could be applied to other hospitals where resources for nosocomial infection surveillance are scarce. The total cost of data collection for this surveillance tool per ward was US$43 per month to motivate physicians to collect 30 min per day of data and to cover the costs of paper forms and a hand calculator. Although our particular interest was in respiratory infections, this strategy could be used to identify other disease syndromes.

These hospitals were frequently overburdened with patients. Wards with higher bed occupancy rates seemed to pose increased risk to patients. Placing patients with emerging respiratory diseases, such as severe acute respiratory syndrome or influenza, on crowded wards without effective infection control procedures creates the potential for large outbreaks of novel respiratory disease, which could pose local, regional, and possibly global threats. In addition, seasonal outbreaks of influenza or episodes of respiratory syncytial virus in hospitals pose a significant threat to vulnerable patients on these wards [23– 25]. Although this surveillance tool could be used to simply alert authorities to possible outbreaks, best practices for response to respiratory disease outbreaks in resource-poor settings are not well defined. Therefore, this surveillance tool could also be used to test interventions within reach of these institutions, such as cohorting, increased ventilation, limiting visitors, or increased handwashing, and draw conclusions about which are the most effective at preventing hospital-acquired respiratory illness in these settings.

Health care workers were part of 18 of the 22 disease clusters we identified, although the number of health care worker illnesses we report are likely underestimates. Physicians working on study wards reported that limited communication between physicians and other staff hindered reporting in both directions. Health care workers in the adult ward of hospital B were 3 times more likely to report illness than those on other wards, and clusters were reported in all but 1 month on that ward. Our data suggest that health care workers are likely at risk of acquiring respiratory infections in the hospitals, and their in fections may pose a risk to other patients or to community members.

Our findings are limited by the sensitivity of our case definition; we only captured illnesses with onset after 72 h in hospital and before patient discharge, and most patients (66%) left the hospital <72 h after admission. In addition, it is possible that patients who were unable to verbalize new symptoms, including children, may have been underreported here, and this, in part, could account for lower rates in pediatric wards compared with adult wards. Respiratory disease is a leading cause of hospitalization in children, which means that fewer children may be at risk for developing respiratory symptoms, and this may also explain lower incidence in pediatric wards. These points suggest that our estimates of hospital-acquired respiratory illness are minimum estimates. It is possible that patients with new onset of respiratory symptoms after 72 h of hospitalization could represent progression of disease in patients admitted with respiratory disease; however, because most of the admitting diagnoses were not for respiratory disease, we believe this phenomenon had little effect on our rate estimates. Finally, our findings are limited by the absence of laboratory testing, which makes it difficult to draw conclusions about the causes of these infections or suggest pathogen-specific prevention measures. Studies to determine the pathogen responsible for clusters of disease, in particular, would be useful for planning interventions.

Prevalence and incidence rates of infection generated by our study are not easily compared with data from other countries; most report hospital-acquired pneumonias or device-associated pneumonias as opposed to more general respiratory disease. Ventilator-associated pneumonia is not a problem in our study hospitals because they do not own ventilators. However, studies from lower-income countries that report all-cause prevalence of hospital-acquired infections suggest that 6–13 of every 100 patients admitted develop a new infection in the hospital and that new respiratory infections occurred in 1.2-3.9 of every 100 patients admitted [2, 4, 5]. Our prevalence estimates for respiratory disease were 0.5-5 per 100 patients admitted per ward, suggesting that hospital-acquired respiratory infections in our study hospitals were similar to other facilities with published rates. Despite the high rates noted in our study, there are certain characteristics of hospital wards we evaluated that might differ from other hospital settings and may reduce the risk of hospital- acquired respiratory infections. Wards were typically well ventilated by ceiling fans and open windows, which may reduce transmission of respiratory pathogens [26]. In addition, family members typically provided most of the hands-on care to patients [27], which limits the opportunities for transmission of disease from one patient to another by hospital staff. Finally, the mean hospital stays for a patient admitted to these wards was only 3.3 days, limiting the amount of time each patient is potentially exposed in the hospital [28].

This surveillance pilot study was started with initiatives by local researchers and donors not local hospitals. There are multiple reasons why this surveillance is unlikely to be adopted by local hospitals without outside support and funding. First, until now, there were insufficient data describing the burden of hospital-acquired infections on which to make decisions about how to prioritize them in these hospitals. Second, there are also no evidence-based interventions that have been shown to reduce respiratory infections in hospitals with scarce resources. Without clear guidance on how to respond, these hospitals are unlikely to find the data generated to be immediately meaningful. However, there are often instances where donors or others in the public health community may be interested in supporting surveillance for hospital-acquired respiratory infections, such as during the current novel H1N1 pandemic, and this strategy may be useful in those situations. Most importantly, this strategy could also be used to gather data about which interventions would work best in these hospitals to reduce the burden of hospital-acquired respiratory disease.

Hospital-acquired respiratory disease poses a threat in our study hospitals for patients and health care workers, and the impact on patient outcomes remains unknown. Additional studies to more precisely measure the burden of hospital-acquired respiratory illness are needed. In-depth studies to better understand infection control challenges and opportunities in these settings are required to develop feasible infection control interventions to reduce risk. Data from our study can be used to engage health authorities and policymakers in discussions about infection control, but this is only a first step in implementing solutions.

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Acknowledgments

The ICDDR,B acknowledges with gratitude the commitment of the CDC to our research efforts. We acknowledge the courageous physicians and health officials at Suhrahwardy Hospital, Rajshahi Medical College Hospital, and Faridpur Medical College Hospital who fearlessly engaged the issue of hospital-acquired infections in their facilities. We appreciate the efforts of our primary collaborators, Rafiqul Islam, Enamul Karim, and A. R. M. Saifuddin Ekram, and our study physicians, Shamim Ferdous Khan, Md. Mahmud Monwar, and Farah Imrana. We greatly appreciate the thoughtful comments and suggestions provided by Eduardo Azziz-Baumgartner on the manuscript and the efforts of Mejbah Uddin Bhuiyan in data collection and cleaning.

Financial support. CDC (cooperative agreement U01 CI000298).

Potential conflicts of interest. All authors: no conflicts.

  • Received June 22, 2009.
  • Accepted December 2, 2010.
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  1. Clin Infect Dis. (2010) 50 (8): 1084-1090. doi: 10.1086/651265
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