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15 November 1996 | Volume 125 Issue 10 | Pages 826-834
Background: Health care workers are at occupational risk for a vast array of infections that cause substantial illness and occasional deaths. Despite this, few studies have examined the incidence, prevalence, or exposure-associated rates of infection or have considered infection-specific interventions recommended to maintain worker safety.
Objectives: To review all recent reports of occupationally acquired infection in health care workers in order to characterize the type and frequency of infections, the recommended interventions, and the costs of protecting workers. Part I of this two-part review focuses on the historical and ethical aspects of the problem and reviews data on infections caused by specific airborne organisms.
Data Sources: A MEDLINE search and examination of infectious disease and infection control journals.
Data Selection: All English-language articles and meeting abstracts published between January 1983 and February 1996 related to occupationally acquired infections among health care workers were reviewed. Outbreak- and non-outbreak-associated incidence and prevalence rates were derived, as were costs to prevent, control, and treat infections in health care workers.
Data Synthesis: More than 15 airborne infections have been transmitted to health care workers, including tuberculosis, varicella, measles, influenza, and respiratory syncytial virus infection. Outbreak-associated attack rates range from 15% to 40%. Most occupational transmission is associated with violation of one or more of three basic principles of infection control: handwashing, vaccination of health care workers, and prompt placement of infectious patients into appropriate isolation.
Conclusions: The risk for occupationally acquired infection is an unavoidable part of daily patient care. Infections that result from airborne transmission of organisms cause substantial illness and occasional deaths among health care workers. Further studies are needed to identify new infection control strategies to 1) improve protection of health care workers and 2) enhance compliance with established approaches. As health care is being reformed, the risk for and cost of occupationally acquired infection must be considered.
In contrast, health care workers who die of occupationally acquired illnesses receive little public attention. Yet, the Centers for Disease Control and Prevention (CDC) calculates that one occupationally acquired disease—hepatitis B—causes 125 to 190 deaths annually among health care workers in the United States [3]. Another calculation projects that 22 health care workers who acquired hepatitis B in 1994 will eventually die of the disease [4]. In recent years, health care workers have also died of occupationally acquired human immunodeficiency virus infection [5] and drug-resistant tuberculosis [6]. Extensive illness results from numerous other occupationally acquired infections. Rather than receiving displays of public sympathy, however, health care workers with occupationally acquired diseases may be neglected or ostracized, their health care benefits imperiled [7, 8].
More than 10 years have elapsed since the last major consideration of this topic [9, 10], although reviews [11-22] and some prospective studies [23-33] have appeared in the interim. During this period, however, much has changed about occupationally acquired diseases. New infections have been identified, diagnostic tests for previously recognized diseases have been improved, and outbreak investigation has come to rely increasingly on molecular analysis. Moreover, at a time when hospitalizations are significantly shorter and more care is delivered outside the hospital, the groups of health care workers at risk have shifted [34-36].
Despite these changes, interventions to prevent or control occupationally acquired infection have been altered very little. Three relatively simple and cost-effective strategies—handwashing, vaccination, and prompt placement of potentially infectious patients into appropriate isolation—have been recognized and advocated for decades. Compliance with these approaches, not knowledge of the approaches themselves, has been conspicuously lacking.
To determine which infections pose risk and how risky specific exposures may be, I reviewed the English-language literature on occupationally acquired infections in health care workers. In the first part of this review, I examine historical and ethical considerations and then characterize the type and frequency of diseases caused by various airborne organisms, including tuberculosis, varicella, measles, influenza, and respiratory syncytial virus infection. The recommended interventions and the costs to protect workers are then appraised. The risks inherent in health care delivery should be considered by planners of health care for the next century.
Other illnesses similarly failed to inspire the heroic among health care workers. Valsalva, Morgagni, and Laennec refused to do autopsies of those dying of tuberculosis for fear of catching the disease [51] (a justifiable concern; Laennec, among many other physicians, was destined to die of tuberculosis). In the early 20th century, scarlet fever and diphtheria comprised half of all infections treated in hospitals [52-58], and as many as 5% of staff members contracted these diseases as a result of occupational exposure [56]. Richardson noted that "many nurses avoid as far as possible the care of such cases ... they fear the possible consequences" [53]. Infection control interventions, including gauze masks for scarlet fever and vaccination for diphtheria, successfully controlled the problem [56].
In 1847, a Code of Ethics written by the fledgling American Medical Association declared it the physician's duty to "face the danger" of caring for the contagious even "at jeopardy of their own lives" [37]. A 1957 revision of the Code, however, not only deleted this section but asserted the physician's right to be "free to choose whom to serve," suggesting that refusal to provide care was acceptable [37]. REVIEW
Occupationally Acquired Infections in Health Care Workers: Part I
Life-threatening risk is a prominent feature of many jobs. In the United States in 1994, approximately 157 policemen [1] and 100 firefighters [2] died in the line of duty. The funerals of many were major public events: Politicians attended, special funds were established for the families of the deceased, and the news media intensively covered the proceedings.
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A literature search was conducted using MED-LINE and volume-by-volume scrutiny of infectious disease and infection control journals. All articles related to occupationally acquired infections in health care workers that were published between January 1983 and February 1996 were reviewed. Abstracts from infectious disease and infection control meetings were also reviewed. Classic articles pertaining to fundamental concepts in transmission and infection control were included when appropriate.
Historical Overview
The emergence of the acquired immunodeficiency syndrome epidemic prompted several examinations of the physician's professional obligation to treat patients who may be contagious. The perspectives taken in these examinations have included the historical, the ethical, and the legal [37-50]. When confronted with the plagues of past centuries, physicians have exhibited behavior that has been anything but exemplary. Galen fled at the height of the Roman plague [37]. In other outbreaks, physicians who could not flee did the next best thing: They "locked themselves into their houses and refused to come out" [37]. Cities responded by hiring "plague doctors" who, in exchange for salary, home, and citizenship, stayed behind to treat the infected [37].
Airborne Transmission
For many diseases, the airborne route was not established as a means of transmission until the 20th century, when the work of Wells and colleagues [59], Riley and associates [60], and others showed that the organisms causing diseases such as measles and tuberculosis were transmitted through the air (Table 1). Transmission may occur in one of two ways. It can occur through inhalation, as with tuberculosis or measles; patients with relevant conditions should be placed in airborne precautions isolation (mask; appropriate ventilation) [93]. Alternatively, it may occur through the autoinoculation of expectorated infectious microorganisms onto the conjunctivae, nasal mucosa, or mouth, as with respiratory syncytial virus infection and the common cold. Patients with these infections should be placed in droplet precautions isolation (mask; possibly gloves, gowns, and goggles) [93].
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Tuberculosis
A disturbing increase was seen in the number of cases of tuberculosis from 1988 to 1992, but the incidence of this disease in the United States has decreased 14.5% over the last 4 years to fewer than 23 000 cases annually [100]. Appreciation of the high rates of acute disease in urban areas, a vastly improved public health infrastructure in many cities, and more vigorous use of standard infection control strategies contributed to this reduction.
Several reviews of tuberculosis and the health care worker have been published [51, 61, 101-103]. A consensus that caring for patients with tuberculosis incurred risk emerged in the 1940s, with the publication of the results of prospective studies done in nursing and medical students [51]. In five representative series, 906 of 1053 susceptible nursing students (86%) developed positive results on tuberculin skin tests and 209 (20%) contracted tuberculosis [61]; these rates far exceeded those in age-matched controls.
Although only about 5% of the U.S. population is estimated to have positive results on tuberculin skin tests [104], the rate is approximately 40% among urban health care workers [61]. Rates of tuberculin reactivity are higher among health care workers who are foreign-born [105] or who have previously been vaccinated with bacille Calmette–Guérin [105]. Moreover, they may have increased risk related to cumulative occupational exposure [106]. Conversion rates among health care workers vary from less than 1% in areas with low incidence rates of tuberculosis (where rates of community-based transmission may exceed rates of nosocomial transmission [107, 108]) to 3% to 4% in hospitals that treat many patients with tuberculosis (where occupational risk is greater [109, 110]). In recent studies [64-66], employees with the highest rates of tuberculin conversion have included housekeeping, laundry, and dietary workers (approximately 8% per year before interventions) and nurses (approximately 4% to 8% per year). Recommended interventions have decreased conversion rates substantially in some but not all groups [64].
In tuberculosis outbreaks, 20% to 50% of susceptible workers may become infected [6, 61, 111]. During recent outbreaks of multidrug-resistant tuberculosis, many workers developed active disease and several died [6, 61]. The CDC has issued guidelines for decreasing spread in health care facilities, and recommended a hierarchy of measures, including the use of administrative and environmental controls as well as the use of personal protective equipment [67]. After analyses showed that preventing one case of occupational tuberculosis would cost $1.3 to $18.5 million [112] and preventing one death would cost $100 million [113], initial plans to require the use of high-efficiency particulate air filter respirators were withdrawn and less costly equipment was approved [114]. Early identification and treatment of suspected cases of tuberculosis is essential and cost-effective [115].
The cornerstone of hospital tuberculosis control efforts is the testing of employees every 6 to 12 months [67]. A 6-month course of isoniazid (300 mg/d) is then administered to new converters of any age and to persons 35 years of age or younger who have a newly identified positive result on a tuberculin test. Optimal prophylaxis for persons exposed to isoniazid- and rifampin-resistant tuberculosis remains uncertain but should include two drugs to which the isolate of the source case was susceptible [67]. The role of bacille Calmette–Guérin vaccine continues to be debated 70 years after its introduction [116-118].
Varicella
About 3.7 million cases of chickenpox occur annually in the United States [119], resulting in high rates of seropositivity among adults. In 1989, 93% of tested U.S. Army recruits were positive for the varicella-zoster virus [120]. The 1994 introduction of an effective vaccine will substantially alter the epidemiology of varicella.
Determining the rates and routes of varicella transmission was the objective of many early studies [55, 121, 122]. Among 11 000 inhabitants of Gloucestershire, England, varicella developed in 61% of susceptible household contacts, measles developed in 76%, and mumps developed in 31% [121]. An outbreak in Boston showed conclusively that varicella-zoster virus was spread through the air [123], a fact that was underscored by transmission to a health care worker who was walking in the hallway outside of an isolated patient's room [124].
Of all health care workers, 2% to 5% are susceptible to varicella-zoster virus [68, 125, 126]. Of those with no known history of varicella, 28% are susceptible [68]. Varicella may develop in apparently immune staff members [127]. The annual incidence of chickenpox among susceptible staff members has ranged from 4.4% [68] to 14.5% [69]. Nurses from areas in which varicella is not endemic are a particular concern [69, 128].
Outbreaks of varicella are a notorious problem for hospital infection control staff [129]. Alternative approaches to furloughing exposed, susceptible employees have been proposed, such as the deliberate exposure of susceptible persons combined with preemptive administration of acyclovir [130] and mandatory wearing of masks by susceptible staff members for 10 to 21 days after exposure [125]. Outbreak investigation may cost $18 000 to $41 000 [131-135]. Annual costs of a prevention program may exceed $55 000, including the costs of replacing workers on furlough, serologic testing, patient isolation, administration of varicella-zoster immune globulin, and infection control time [134]. The newly available varicella vaccine has recently been recommended [70] for susceptible health care workers. The cost of identifying and vaccinating susceptible employees, the risks of administering a live vaccine, and the possible spread of vaccine-induced disease all must be considered when an employee vaccination program is implemented [19].
Measles
Decades ago, 500 000 cases of measles were seen annually in the United States. The 1963 introduction of an effective vaccine and the recognition of the need for an additional vaccination after infancy resulted in a decrease to 5000 cases annually [119]. Outbreaks, which usually affect high school or college students, continue to occur and serve to reemphasize the importance of an active vaccination program.
Health care workers are the source of 5% to 10% of all cases of measles [71, 72, 136-140]. A visit to a medical setting [136-138], particularly a pediatric emergency department [140, 141], increases the risk for measles, and a case of measles acquired nosocomially may be more severe than an ordinary case [142, 143]. Spread may begin in a hospital and then enter the community [144].
Five percent to 10% of health care workers are susceptible to measles [145-149]. The rate is age-dependent: Sixteen percent of health care workers born in the 1960s and 34% of health care workers born in the 1970s are susceptible [71, 150, 151]. Health care workers account for 28% of cases of measles in medical settings in the United States [71, 139]; nurses and physicians make up half of the affected persons. Workers acquire measles through exposure to patients (91%) or other health care workers (9%) [71].
Vaccination is recommended for persons born after 1957. In one survey, however, 29% of cases of measles seen in health care workers occurred in persons born before 1957 [139], suggesting that this age-based criterion may not be useful in high-risk populations [149]. Targeted vaccination of health care workers known to be susceptible is less costly than vaccinating all workers [147, 150]: $23 000 compared with $71 000 [150]. Although vaccines can fail [152, 153], breakthrough cases of measles are often milder than other cases [152].
Influenza
Outbreaks of influenza occur each winter in the United States and cause substantial illness. An effective vaccine has been available since the 1950s and may be indicated even for adults without underlying medical conditions [154]. Nonetheless, rates of vaccination for patients and health care workers remain woefully low, lower than 50% in some series [75].
Numerous nosocomial outbreaks of influenza have been reported [73, 74, 155-162]. During the epidemic of 1918-1919, more than 40 nurses and many physicians at New York Hospital developed influenza, and 1 nurse died [155]. Nationally, however, no disproportionate increase in cases of influenza in health care workers was shown [43]. During the 1957-1958 outbreak, 15 of 33 health care workers on one ward (45%) developed influenza, including 7 persons who had been vaccinated [73].
Recently reported outbreaks have involved large numbers of employees. In one, influenza spread to 118 workers, including 8% of the nurses and 3% to 6% of the physicians at a hospital with poor vaccination compliance rates [74]. In another, 43% of nursing students had a flu-like illness [157]. Employee absenteeism is an indirect way to assess the effect of influenza [158]: At one hospital, absenteeism during a community outbreak was 1.7 times higher than it had been the year before, costing an additional $24 500 for sick leave. Because cases of influenza B may be mild, outbreaks can be difficult to detect [159]. In an outbreak of influenza B at a nursing home [160], 59% of staff members missed work because of a flu-like illness.
Strategies to improve compliance have been ineffective [75], and vaccine failure occurs [73, 161, 162]. In one report, no virus was transmitted to 28 unvaccinated employees who were exposed to an unisolated patient for a mean of 4 hours [162]. Despite having been vaccinated, the patient's primary physician developed influenza, presumably because of more prolonged exposure.
Rubella
Ten percent to 20% of hospital personnel are susceptible to rubella [163, 164]. Because rubella can affect fetal development, rubella outbreaks are particularly dramatic. In an outbreak in Boston, 13% of all health care workers developed clinical rubella (47 cases) [76], additional subclinical cases occurred, and 500 work days were lost. One health care worker opted to terminate her pregnancy. In Los Angeles [77, 164], 56 employees developed rubella and 3 terminated pregnancies. An outbreak at a dental school involved 17 persons [165]. Children with congenital rubella may shed virus chronically and may therefore remain contagious [166]. The need for employee vaccination is underscored by numerous outbreaks in which health care workers have been source cases [72].
Mumps
As a result of vaccination and herd immunity, mumps is now less common than it used to be. However, 15.6% of U.S. Army recruits [120] and 6.8% of medical students [167] are susceptible, and outbreaks occur in vaccinated populations [168]. In a prevaccine survey of 9299 persons, the incidence of mumps was highest among health care workers [78]: Rates were 15% for physicians (37% for pediatricians) and 18% for dentists. In comparison, rates were 9% for elementary school teachers and 2% for university staff members. During an outbreak of mumps in Tennessee in 1986-1987 [169], at least 6 health care workers developed mumps after nosocomial exposure. Placing patients with mumps into respiratory isolation may fail to prevent transmission [79, 80].
Pertussis
The number of cases of pertussis in the United States has increased nationwide since the early 1980s [119]. Estimates suggest that 25% of vaccinated persons may be susceptible [170], and outbreaks have occurred in vaccinated populations [82]. At least seven outbreaks have involved health care workers [83]. In a facility for the disabled [81], 42 of 107 exposed workers (39%) became infected. Erythromycin (1 to 2 g/d for 2 weeks) is effective prophylaxis [81, 83]. Clarithromycin or trimethoprim-sulfamethoxazole is a potential alternative [83]. Use of acellular vaccine during outbreaks appears to be safe [171].
Parvovirus B19 Infection
Parvovirus B19 is responsible for "fifth disease," aplastic crisis in patients with sickle-cell disease [172], and hydrops fetalis [173]. About half of adults are immune [174, 175]. In nonoutbreak settings, the risk of school employees is 13 times higher than that of hospital workers [175]. In an outbreak in a pediatric hospital, 12 of 32 susceptible health care workers (38%) developed disease [84]. Rates of infection were highest among nurses who were exposed to nonisolated patients soon after admission and exceeded those reported from family-based outbreaks [176] and outbreaks in day care centers [177, 178]. Outbreak-related incidence rates ranging from 27% to 47% have been described in an adult ward [85], a developmental center [86], and a neurosurgical intensive care unit [87]. A normal child was born to an employee who became infected while pregnant [88]. One study found that no transmission had occurred, possibly because the source case was a chronic secretor with a relatively low viral load [179]; another suggested that community-based transmission had a significant role [180].
Respiratory Syncytial Virus Infection
Community outbreaks of respiratory syncytial virus infection occur predictably during most winters and may enter hospitals. Determining the best way to interrupt nosocomial spread has been the subject of numerous studies [90-92, 181-185]. In one outbreak [89], 10 of 24 health care workers (42%) developed disease. Thereafter, implementation of infection control procedures, including handwashing, use of gloves and gowns, and isolation, effectively decreased spread among patients but not among staff members: Twenty-four of 43 health care workers (56%) developed disease the next year [90]. Cohorting patients with respiratory syncytial virus infection appears to be a safe practice [184-186]. Masks are not clearly beneficial [181].
Adenovirus Infection
Adenovirus has spread to staff members during outbreaks at ophthalmology clinics [96-98], intensive care units [95, 99], pediatric long-term care facilities [94, 187], and nursing homes [188]. Intubating patients with adenovirus pneumonia may facilitate transmission. In one outbreak that arose from a patient with fatal adenovirus pneumonia, adenovirus type 4 spread to 9 of 23 workers (39%) [95], and at least 23 employees developed adenovirus type 3a infection in a similar outbreak [99]. Health care workers in both outbreaks developed self-limited disease. At a long-term pediatric facility, 23 of 106 workers developed adenovirus during an outbreak. The highest rate was seen among nurses, particularly those who were responsible for suctioning children [94]. Molecular epidemiologic techniques have helped confirm the occurrence of several outbreaks [99, 187].
Other Infections
In one report, hand-foot-and-mouth disease affected 17 of 136 operating suite personnel (13%), including 11 nurses [189], and cost $5676 and 82 work days. Diphtheria developed in an intern during an ongoing outbreak [190]. The occupational risk for legionnaires disease [191] and hantavirus infection [192, 193] is low. Spread of mycoplasma to 44% of 97 staff members was detected using a molecular hybridization test; two workers developed pneumonia [194]. Parainfluenza spread to 18 of 52 nurses in one outbreak (35%) [195]. Three workers developed symptomatic group A streptococcal disease after exposure to one patient [196]. Rhinovirus accounted for many occupationally acquired infections in early surveys [197]. Subsequent studies emphasized the effectiveness of handwashing in limiting spread [198, 199]. Occupationally acquired cases of typhus [155] and smallpox [200-202] have been reported.
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