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Am. J. Trop. Med. Hyg., 75(1), 2006, pp. 36-40
Copyright © 2006 by The American Society of Tropical Medicine and Hygiene

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NATIONAL SURVEILLANCE AND THE EPIDEMIOLOGY OF HUMAN Q FEVER IN THE UNITED STATES, 1978–2004

JENNIFER H. McQUISTON*, ROBERT C. HOLMAN, CANDACE L. McCALL, JAMES E. CHILDS, DAVID L. SWERDLOW, AND HERBERT A. THOMPSON
Viral and Rickettsial Zoonoses Branch and Office of the Director, Division of Viral and Rickettsial Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia


ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Although Q fever is considered enzootic in the United States, surveillance for human Q fever has been historically limited. From 1978 through 1999, 436 cases (average = 20 per year) of human Q fever were reported. After Q fever became nationally reportable in 1999, 255 human Q fever cases (average = 51 per year) were reported with illness onset during 2000 through 2004. The median age of cases was 51 years, and most cases were male (77%). The average annual incidence of Q fever was 0.28 cases per million persons, and was highest in persons 50–59 years of age (0.39 cases per million). State-specific incidence ranged from a high of 2.40 cases per million persons in Wyoming, to 0 cases in some states. Since Q fever became reportable, case reports have increased by more than 250%. Surveillance for Q fever is essential to establish the distribution and magnitude of disease and to complement U.S. bioterrorism preparedness activities.


INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Coxiella burnetii, which causes the zoonotic disease Q fever, occurs worldwide and has been found in a wide range of domestic and wild mammals, numerous species of ticks, and several avian species. Ruminants are considered the primary reservoir, and human infections are usually acquired after contact with infected animals, especially sheep, cattle, and goats. However, other animals, including cats, dogs, and wildlife, are also sometimes associated with human infections.1 Identifying the source of human infection is sometimes difficult because infection in animals is usually asymptomatic or limited to abortion and production losses.2 Coxiella burnetii is shed in birthing fluids and byproducts of parturition, milk, and feces from infected animals. Once these infectious materials contaminate the environment, the organism can survive for several weeks, and is resistant to desiccation and temperature extremes. The most common route of transmission from infected animals to humans is inhalation of aerosols or dust containing C. burnetii. Consumption of unpasteurized dairy products may also result in human infection.1 Tick-bite and sexual transmission have been implicated on rare occasions.3,4

Acute human infection presents as a febrile illness 1–3 weeks after exposure to C. burnetii. Initial clinical signs are nonspecific and include headache, myalgias, cough, fatigue, and night sweats.5–7 Approximately one-third of patients may develop acute respiratory disease, and up to two-thirds of patients may have hepatic involvement. Abortion may occur in pregnant women.8 Rare serious complications of acute infection include meningoencephalitis and myocarditis. Approximately 10% of patients report symptoms of chronic fatigue for months to years after acute infection,9 and a small percentage of patients develop chronic infection characterized by granulomatous hepatitis, osteomyelitis, or culture-negative endocarditis. Persons with pre-existing heart valve abnormalities, artifical valves, or immunosuppressive conditions are at higher risk for the development of endocarditis after acute infection.5

Although Q fever is considered enzootic in ruminants in the United States, the epidemiology of human Q fever infections in this country is poorly understood. The last national surveillance study that provided information on cases reported by states described 1,168 cases during 1948 through 1977 (average = 39 per year).10 Sporadic Q fever case reports and descriptions of outbreaks have been published, and when examined collectively, these suggest that sheep play an important role in the epidemiology of human Q fever infection in the United States.11 However, widespread serologic evidence of infection in cattle suggests that the role of these animals in human infection may be under-appreciated.11 Seroprevalence studies in humans in the United States suggest that persons with occupational contact with livestock (veterinarians, farmers, slaughterhouse workers) are seropositive at a rate 10 times greater than the general population. However, because these studies focus on detection of antibody rather than active infection, and are both geographically and temporally limited, they do not provide an accurate assessment of incidence.11

Emerging concerns over the potential use of C. burnetii as a bioterrorism agent prompted U.S. officials to add Q fever to the national list of notifiable diseases in 1999.12,13 It is important to understand both the historical and current incidence of disease to establish a baseline against which bioterrorism surveillance may be compared. This study provides a historical Q fever case count from 1978 through 1999, and provides a current national summary of the epidemiology of Q fever in the United States during 2000 through 2004.


MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Collection of surveillance data. The Centers for Disease Control and Prevention (CDC) conducted a retrospective survey of state health departments in 2002 to collect information on human Q fever cases reported for 1978 through 1999. Q fever case information for cases with illness onset during 2000 through 2004 were obtained through the National Electronic Telecommunications System for Surveillance (NETSS).14 Through NETSS, state health departments submit electronic case reports to the CDC for all reportable diseases. These data include the first five complete years of cases after the addition of human Q fever to the national list of notifiable diseases in 1999.13 Data available through NETSS included date of illness onset, sex, age, race/ethnicity, and reporting state for each case. Although available through NETSS, county-level data were not included in this report due to confidentiality concerns and restrictions in reporting for rare diseases. We included cases in this study reported to NETSS as confirmed or probable Q fever; suspect cases were excluded. Case status was assigned by state health departments, and was assumed to have been based upon the currently approved CSTE case definition.13 The annual number of cases presented in this report are based on the year of illness onset. A small number of cases had their NETSS reporting year different than their year of illness onset (i.e., cases had a delayed diagnosis or were reported to NETSS restrospectively); therefore, the annual number of cases may be slightly different than those published NETSS summary reports.15–18

Incidence was calculated as the number of reported Q fever cases per 1,000,000 persons per year.19,20 Incidence calculations were limited to NETSS-reported cases for 2000 through 2004, corresponding to years in which Q fever was considered a reportable disease by national authorities. Incidence calculations were further restricted to years for which Q fever was considered reportable at the state level. For example, if a state added Q fever to its reportable disease list in 2002, only 2002 through 2004 reporting and census data contributed to state and national incidence calculations. Comparisons of categorical data between groups were made by chi-square test or Fisher’s exact test (two-tailed), as appropriate. The age distribution of cases during 2000 through 2004 was compared with the U.S. age distribution for the same period using the chi-square test of goodness of fit.

Diagnosis of Q fever. Because Q fever presents as a relatively nonspecific illness, clinical criteria alone cannot be relied upon to provide accurate surveillance data. Diagnosis of C. burnetii infection in humans relies on detection of the organism in affected tissues or demonstration of developing immunity through serologic assays. Serologic tests are most commonly used to diagnose human C. burnetii infections in the United States.21 A four-fold change in antibody titer to C. burnetii antigen was considered indicative of a confirmed case of Q fever, and elevated single titers or standing titers to C. burnetii antigen were supportive of probable Q fever cases.13 During 1978 through 1999, the types of serologic assays available for the diagnosis of Q fever in humans varied. Prior to the 1990s, the complement fixation test was the most widely used serologic assay. During 2000 through 2004, the period in this report, the indirect immunofluorescent antibody assay was the standard serologic test available in the United States.21


RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Between 1978 through 1999, 436 cases of Q fever in humans were recognized and reported by state health departments in the United States (Table 1Go). The mean number of annual cases reported during this period was 20 (range = 6–41) (Figure 1Go).


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TABLE 1
Number of cases and average annual incidence of human Q fever by state, United States, 1978–1999 and 2000–2004
 

Figure 1
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  		    FIGURE 1. Annual number of cases of Q fever in humans reported by state health departments, United States, 1978–2004 *Years in which Q fever was a nationally reportable disease.

 
During 2000 through 2004, the first five years during which Q fever was nationally reportable, 255 cases were reported from 37 states and the District of Columbia (Table 1Go). The average annual number of reported cases was 51 cases (range = 18–73). Cases were seasonal, with 99 (39%) reported in April through June (Figure 2Go). Sex was reported for 252 cases, of which 195 (77%) were male. Age at illness onset was reported for 254 cases; the mean age at Q fever onset was 50.5 years and the median age was 51 years. There was no significant difference in sex distribution between adolescents (age < 18 years) and adults (age ≥ 18 years) (P = 0.32). Of 171 cases with information on race and ethnic background available, 157 (92%) cases were white, 11 (6%) were black, and 3 (2%) were Asian. The proportion of different races affected by Q fever was similar to the expected race proportions in the general U.S. population during this time period. Of 167 cases reporting ethnicity, 23 (14%) cases indicated they were Hispanic, similar to the proportion of Hispanics in the general U.S. population.


Figure 2
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  		    FIGURE 2. Percent of total Q fever cases by month of illness onset, United States, 2000–2004.

 
For 2000 through 2004, the national average annual incidence was 0.28 cases per million persons per year. The age distribution of cases was significantly different than that of the general U.S. population (P < 0.0001). The average annual incidence increased with age, peaking in the 50–59-year-old age group (0.39 cases per million persons) (Figure 3Go).


Figure 3
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  		    FIGURE 3. Annual incidence of Q fever by age group, United States, 2000–2004.

 
State-specific incidence ranged from a high of 2.40 cases per million persons (Wyoming) to 0 reported cases per million persons in some eastern states (Figure 4Go). Although California reported the highest number of human Q fever cases during 2000 through 2004 (n = 48), the state had a moderate incidence of 0.35 cases per million persons. Several Q fever cases were reported from predominantly urban centers, including the District of Columbia (n = 3) and New York City (n = 5). These cases appeared isolated and did not cluster in time.


Figure 4
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  		    FIGURE 4. Average annual incidence of Q fever by state, United States, 2000–2004.

 

DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Prior to 1978, there had been few national surveillance summaries that provided information on human Q fever infections in the United States. The only previous summary to provide state-specific information on human Q fever infections reported numbers of cases occurring from 1948 to 1977, and did not report trends over time or epidemiologic features of disease.10 The renewed interest in C. burnetii as a possible agent of bioterrorism has highlighted the need to more accurately understand the disease burden of Q fever in the United States, and prompted the current review of surveillance data from 1978 through 2004.12

In this study, the average annual incidence for states reporting Q fever was calculated to be 0.28 cases per million persons, with state-specific incidence ranging from 0.0 to 2.40 cases per million persons per year. The average annual incidence in England and Wales is similar to that observed in the United States, with average annual incidence of 2 cases per million persons.22 In contrast, the annual incidence of Q fever in some regions of France has been estimated to be as high 500 cases per million persons, and the estimated annual incidence in Australia is approximately 38 cases per million persons.1,5,23

The low reported incidence of Q fever in the United States compared with France and Australia is striking. Most human Q fever cases in France and Australia are epidemiologically linked to exposure to small ruminants (sheep, goats, or their unpasteurized milk products), which make up an important part of the agricultural industry in those countries.1,5,23 In contrast, agriculture in the United States is heavily weighted toward the beef and dairy cattle industries rather than small ruminant farming.24–26 Thus, the circumstances of human exposure to C. burnetii are likely different in the United States than occurs in France and Australia.

The epidemiologic features of human Q fever in the United States for the period 2000 through 2004 were similar to those reported in other countries.5,22,23 Cases appeared seasonal, with 39% of cases occurring from April to June; however, cases were reported throughout the year, suggesting that human Q fever infections may also have non-seasonal influences. In France and England, human Q fever cases are primarily reported in April–June after a period where lambing frequently occurs outdoors.5,22 In contrast, cases in Australia do not show a distinct seasonal trend.23

Similar to other published reports, Q fever in the United States occurs more frequently among males than females. Recent studies have suggested that among adults, susceptibility to infection with C. burnetii may be influenced by sex hormones, and that females may develop clinical illness less frequently than males because of the protective role of 17ß-estradiol.27 Studies on the epidemiology of Q fever in children have suggested a male:female distribution ratio close to 1.28 We did not observe a significant difference in sex proportions between adolescents and adults; however, the low number of childhood Q fever cases reported through this national surveillance report may have precluded an accurate assessment of this risk factor.

In this surveillance summary, annual average incidence varied by state. Eastern states typically had the lowest incidence of Q fever, ranging from 0.0 to 0.10 per million population. The states with the highest annual incidence (> 0.50 cases per million) included Idaho, Kentucky, North Dakota, Nebraska, Nevada, Oregon, Tennessee, and Wyoming. Although California reported more cases than any other state in both the current surveillance summary and in previously published summaries,10 when human population parameters are taken into account the state has only a moderate incidence of Q fever. Interestingly, urban centers such as the District of Columbia and New York City reported sporadic cases, despite having few opportunities for spread from ruminants. These appeared sporadic in nature and did not cluster by time or location, suggesting that bioterrorism did not play a role. Exposures for some of these cases may have occurred during recent travel, or through contact with contaminated materials imported from disease-endemic areas. In addition, some cases may have been newly diagnosed chronic Q fever infections with prior exposures in other geographic areas.

These data are subject to several important limitations. Q fever was made notifiable in 1999,13 and a maximum of only five years of national reporting data were available to determine state and national incidence, which may not allow an accurate assessment of true incidence. Because Q fever is a rarely reported disease, incidence calculations can be influenced by changes in local or state reporting mechanisms or the occurrence of small focal outbreaks. In addition, because of the small number of reported cases, we were only able to provide overall rates rather than adjusted rates. The symptoms of Q fever are nonspecific, and definitive early laboratory tests do not yet exist. Laboratory serologic analysis is the most widely available assay for Q fever diagnosis, but antibody does not usually appear prior to day seven of acute infection, and analysis and interpretation of results are not easy. Therefore, it must be presumed that many additional cases of Q fever probably occurred in the United States but were not adequately assessed or were not reported to authorities. The NETSS system does not include information on how a diagnosis was made; thus, it is not possible to confirm that all reported cases had supporting laboratory evidence of infection, and some cases may have been incorrectly classified as Q fever. Finally, an accurate assessment of clinical signs and symptoms, fatality rates, and presentation of acute versus chronic infection was not possible with the surveillance data available.

This study provides the first national and state-specific incidence rates for human Q fever infection in the United States, and provides an important baseline assessment by which to compare future surveillance efforts. The 250% increase that occurred in reported Q fever cases between 2000 and 2004 may suggest a trend toward improved recognition and reporting of the disease rather than a change in the actual burden of disease. It will be important to continue surveillance and to periodically re-calculate baseline incidence to help establish a more accurate representation of the endemic burden of disease, and to establish the threshold that may indicate natural or intentional outbreaks of Q fever. Furthermore, although this study was not able to review pertinent risk factors for infection, it is likely that a complex interplay of human, animal, and environmental factors influence the geographic risk for Q fever infection in the United States. Future studies to assess the role of agricultural and livestock population densities, regional farming practices, and climactic factors such as temperature, wind direction, and rainfall may clarify geographic infection patterns.

Received November 16, 2005. Accepted for publication February 28, 2006.

Acknowledgments: We thank the state health departments who freely shared surveillance data.

Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the funding agency.

* Address correspondence to Jennifer H. McQuiston, Division of Global Migration and Quarantine, Centers for Disease Control and Prevention, 1600 Clifton Road, Mailstop E-03, Atlanta, GA 30333. E-mail: fzh7{at}cdc.gov Back

Authors’ addresses: Jennifer H. McQuiston, David Swerdlow, and Herbert A. Thompson, Viral and Rickettsial Zoonoses Branch, Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, 1600 Clifton Road, Mailstop E-03, Atlanta, GA 30333, Telephone: 404-639-1075, Fax: 404-639-2778, E-mail: fzh7{at}cdc.gov. Robert C. Holman, Office of the Director, Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, 1600 Clifton Road, Mailstop A-39, Atlanta, GA 30333. Candace L. McCall, United States Air Force, Air Force Institute of Operational Health, Risk Assessment Division, 2513 Kennedy Circle, Brooks City-Base, TX 78235-5116, Telephone: 210-536-3471, Fax: 210-536-6841. James E. Childs, Department of Epidemiology and Public Health, Yale School of Medicine, 60 College Street, Room 600, PO Box 208034, New Haven, CT 06520.


REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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