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Seroepidemiologic and Occupational Risk Survey for Coxiella burnetii Antibodies among US Veterinarians

  1. Ellen A. S Whitney1,2,
  2. Robert F. Massung3,
  3. Amanda J. Candee3,
  4. Elizabeth C. Ailes1,2,
  5. Lee M. Myers4,a,
  6. Nicole E. Patterson3, and
  7. Ruth L. Berkelman1,2
  1. 1Center for Public Health Preparedness and Research, Agriculture, Atlanta
  2. 2Department of Epidemiology, Rollins School of Public Health, Emory University, Agriculture, Atlanta
  3. 3Rickettsial Zoonoses Branch, Division of Viral and Rickettsial Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases, Centers for Disease Control and Prevention, Agriculture, Atlanta
  4. 4Georgia Department of, Agriculture, Atlanta
  1. Reprints or correspondence: Ms. Ellen A. S. Whitney. Ctr. for Public Health Preparedness and Research and Dept. of Epidemiology, Rollins School of Public Health, Emory University, 1518 Clifton Rd., NE, Atlanta, GA 30322 (ewhitn2{at}emory.edu).

  1. ↵a Present affiliation: National Veterinary Stockpile, US Department of Agriculture Animal and Plant Health Inspection Service, Good Hope, Georgia (L.M.M.).

 
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Abstract

Background. Little is known about the occurrence of Q fever among veterinarians in the United States. In this study, we sought to estimate the prevalence of Coxiella burnetii antibodies among veterinarians and to identify risk factors for exposure.

Methods. We tested serum samples from 508 veterinarians who attended the 143rd American Veterinary Medical Association Annual Convention in 2006. Samples were screened using a Q fever IgG enzyme-linked immunosorbent assay (ELISA). Samples with positive or equivocal results of ELISA were confirmed using phase I and phase II IgG immunofluorescence antibody assays, and end point IgG titers were determined for samples with positive results.

Results. Antibodies against C. burnetii were detected in 113 (22.2%) of 508 veterinarians. Risk factors associated with seropositivity included age ⩾46 years, routine contact with ponds, and treatment of cattle, swine, or wildlife.

Conclusions. Veterinarians have a high level of exposure to C. burnetii, the causative organism of Q fever, especially those veterinarians who treat livestock. In this study, risk of C. burnetii seropositivity was also independently associated with contact with ponds. The role of exposure to standing bodies of water in infection is not usually considered and should be investigated in future studies. Additionally, the evidence of past infection with C. burnetii in >20% of veterinarians also highlights the need for use of appropriate personal protective equipment when treating animals that are potentially infected with C. burnetii. Physicians should consider the risk of infection with C. burnetii when treating ill veterinarians and others with potential occupational exposures.

Little is known about the incidence of zoonotic infections among veterinarians in the United States. Few public health and occupational health studies examining occupational exposures and rates of infection among veterinarians have been conducted. Because most emerging infectious diseases are zoonotic in origin, it is important to understand the risk of infection in individuals who work with animals [1, 2]. One zoonotic infection of concern to veterinarians is Q fever [3].

Q-fever is a zoonotic disease caused by a highly infectious bacterium, Coxiella burnetii. Humans become infected by inhalation of aerosols or contaminated dust from infected ruminants, such as cattle, sheep, and goats, or through exposure to infected animal products [3-5]. Cats, dogs, and wildlife may also serve as reservoirs of C. burnetii [3, 6-9]. Exposure and seroconversion may result from consumption of unpasteurized dairy products [10]. Person-to-person transmission is rare but has been reported through sexual contact and aerosol transmission [11, 12].

From 2000 through 2006, a total of 554 cases of Q fever in the United States were reported to the Centers for Disease Control and Prevention, with a peak of 169 cases reported in 2006. Because many human infections with C. burnetii are mild or asymptomatic, it is likely that many infections are not diagnosed [13, 14]. Acute infection may present as a self-limited influenza-like syndrome; atypical pneumonia or hepatitis may be observed in more-severe cases [11, 14]. Chronic Q fever may develop within several months or years after an acute infection in 5% of patients [14]. In persons with valvular damage, endocarditis may occur [14]. It is estimated that the mortality rate of chronic Q fever ranges from 2% to 65% [14-16]. When appropriately treated with antibiotics, Q fever is rarely fatal [14]. Reactivation of latent Q fever during pregnancy may be associated with spontaneous abortion, placentitis, or thrombocytopenia [17, 18].

We previously conducted a cross-sectional study to assess the seroprevalence of antibodies to Leptospira species among veterinarians [19]. Our interest in zoonotic pathogens that infect veterinarians led us to also consider the risk faced by veterinarians for other zoonotic infections, such as C. burnetii infection. Therefore, we sought to estimate the prevalence of C. burnetii antibodies among veterinarians and to identify risk factors for exposure.

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Materials and Methods

As described elsewhere [19], we conducted a national seroepidemiologic survey of healthy, practicing veterinarians attending the 143rd American Veterinary Association Annual Convention, 15-19 July 2006, in Honolulu, Hawaii. The study was performed with the support of the American Veterinary Medical Association (AVMA) and the Group Health & Life Insurance Trust (GHLIT). Written informed consent and Health Insurance Portability and Accountability Act authorization were obtained from each participant. We collected information on participants' demographic characteristics, animal specialties, clinic experience, reported recent exposures, accidental vaccine exposure, recent illness and injury, and use of personal protective equipment and practices through a self-administered, standardized survey. After the completion of the survey, a single blood sample was collected in a 10-mL serum separator tube from each participant by experienced personnel from LabOne/Quest Diagnostics and sent to Emory University.

In 2007, participants' serum samples were tested for the presence of antibodies against C. burnetii in the Q Fever Laboratory at the Centers for Disease Control and Prevention. Sera were screened using the Q Fever Phase II IgG ELISA (PanBio), according to the manufacturer's protocol. For the assay, sera were diluted 1:100 with Tris-buffered saline (pH, 7.2-7.6), and 100 µL of diluted sera were added to each well of 96-well plates coated with C. burnetii phase II antigen. Positive control, negative control, and triplicate wells with calibrator control sera were used on each plate. Plates were incubated, washed, and developed according to the manufacturer's protocol. Plates were read on a spectrophotometric microplate reader (Victor 2L; PerkinElmer) at a wavelength of 450 nm. Data were analyzed according to the protocol provided by PanBio. Briefly, sample absorbance was divided by the average absorbance of the calibrator control wells, then multiplied by 10 to arrive at “PanBio units.” Samples with calculated PanBio units <9 were considered to have negative results, samples with PanBio units 9-11 were equivocal, and samples with >11 PanBio units were considered to have positive results. Field et al. [20] determined the sensitivity and specificity of the PanBio Q fever IgG ELISA to be 71% and 96%, respectively. Samples that were determined to be equivocal or positive by ELISA were then tested by immunofluorescence antibody assay to obtain end point titers for IgG to both phase I and phase II C. burnetii antigens [21]. Samples with immunofluorescence IgG antibody titers of ⩾1:16 were considered to have positive results.

Survey data were entered into an Access 2003 (Microsoft) database and analyzed in aggregate form with use of SAS, version 9.1 (SAS Institute). For continuous variables, the median value was calculated, and responses were dichotomized as less than or greater than or equal to the median value. These dichotomous variables were used in additional analyses. Comparisons between C. burnetii-seropositive and C. burnetii-seronegative participants were conducted using Fisher's exact test for ordinal and dichotomous variables, where appropriate. Logistic regression was performed to determine the OR comparing the odds of a given exposure among veterinarians seropositive for C. burnetii antibodies with that for seronegative veterinarians. The EXACT statement was used when there were <5 responses per group. Veterinarians who did not enter information for specific questions were excluded from the analysis of that particular question. Variables with 2-sided P values <.1 were selected for multivariable logistic regression. Variables selected for multivariable logistic regression were analyzed for collinearity with use of a SAS macro (SAS Institute) [22]. Backwards, forwards, and stepwise multivariable logistic regressions were performed to select the final multivariable model. The Institutional Review Board at Emory University reviewed and approved this protocol.

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Results

General characteristics of study participants. From 15 July through 18 July 2006, we enrolled 535 participants of the AVMA annual meeting who attended the AVMA GHLIT Wellness Booth. Veterinarians with a doctorate of veterinary medicine who were practicing ⩾50% of the time and provided a sufficient serum sample for serologic testing were eligible for inclusion. Twenty-seven individuals were excluded because they did not meet the inclusion criteria; 508 veterinarians were included in the final analysis.

The age of participants ranged from 25 to 81 years and the median age of all participants was 46 years (interquartile range, 35-54 years). Two hundred fifty-five (50.3%) participants were women and 252 (49.7%) were men. The majority of participants' (87%) primary location of work was in a clinic. Most participants (69.2%) had small animal practices and treated dogs (93.7%), cats (93.7%), rabbits (64.4%), pocket pets (62.4%), and ferrets (55.8%). Overall, 113 (22.2%) veterinarians were found to be seropositive for C. burnetii. Phase I and phase II antibody titers ranged from 1:16 to 1:1024. The median phase I titer was 1:128 (interquartile range, 1:32-1:256). The median phase II antibody titer was 1:128 (interquartile range, 1:64-1:256).

Factors associated withC. burnetii seropositivity in univariate analysis. Seropositive veterinarians were more likely to be men and to be aged ⩾46 years (table 1). Compared with veterinarians with a small animal practice, veterinarians with a mixed small/large animal practice and those with a food animal practice were more likely to be seropositive (table 1). Veterinarians who reported offering mobile veterinary services were more likely to be seropositive (table 1). When stratified analysis of mobile veterinary services by type of practice was performed, veterinarians in small animal practices who offered mobile services were more likely to be seropositive than were those who did not offer mobile services (OR, 2.19; 95% CI, 1.07-4.46; P=.031). No difference was observed between seropositive and seronegative veterinarians who worked at a mixed-animal practice (data not shown). Furthermore, ever living on a farm, currently living on a farm, and exposure to ruminants while living on a farm were associated with seropositivity. Veterinarians who reported treating cattle, exotic livestock, horses, mammalian wildlife, nonhuman primates, poultry, ruminants, or swine were more likely to be C. burnetii seropositive (table 1).

Table 1
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Table 1

Univariate analysis of select variables associated with Coxiella burnetii antibody seropositivity among participating veterinarians.

Veterinarians who reported any routine exposure to bodies of water tended to be seropositive, but the relationship was not statistically significant. However, routine contact with rivers, streams, lakes, and ponds (fresh water) were each significantly associated with seropositivity, as was routine contact with ditch or sewage water (table 1).

Overall, 18 (16%) of the 113 seropositive veterinarians and 68 (17%) of the 395 seronegative veterinarians reported ⩾1 instances of exposure to modified live-vaccine products within the previous year (July 2005-July 2006). Exposure to Brucella species or RB51 vaccine products was significantly associated with C. burnetii seropositivity, whereas exposure to Bordetella species vaccine was protective (table 1). Further analysis of exposure to Brucella species or RB51 vaccine, controlling for the treatment of cattle or with stratification by type of practice, found no statistically significant relationship (data not shown).

Certain occupational practices were found to be associated with C. burnetii seropositivity. Among veterinarians who reported using various personal protective equipment, individuals who reported ever wearing a mask were less likely to be seropositive than were those who reported never wearing a mask (OR, 0.466; 95% CI, 0.264-0.823; P=.009). Veterinarians with mixed small/large animal practices who sometimes wore a mask were less likely to be seropositive than were those who never wore a mask (OR, 0.286; 95% CI, 0.085-0.969; P=.044). In addition, veterinarians who reported always wearing a lab coat or equivalent were statistically less likely to be C. burnetii seropositive (table 2). When the use of lab coat or equivalent was stratified by type of practice, no statistically significant effect was found. Occupational exposures (i.e., needle sticks and accidental cuts) were also found to be associated with C. burnetii seropositivity (table 3). Veterinarians who experiences ⩾2 cuts within the previous year (July 2005-July 2006) were statistically more likely to be seropositive. Forty-one (36%) seropositive veterinarians reported having been stuck by a needle ⩾3 times within the pervious year, compared with 105 (27%) seronegative veterinarians, although this was not significant when compared with those who had no accidental needle sticks within the previous year.

Table 2
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Table 2

Univariate analysis of personal protective equipment and select occupational behavioral practices potentially associated with Coxiella burnetii antibody seropositivity (n=508)

Table 3
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Table 3

Occupational injuries of participating veterinarians within the past year potentially associated with seropositivity to Coxiella burnetii (n=508).

Factors associated withC. burnetii seropositivity in multivariate analysis. Of the variables that were found to be significant at the P<.10 level by univariate analysis, the following variables were associated with C. burnetii seropositivity in the multivariate analysis at a significance level of P<.05: age ⩾46 years (OR, 1.84), routine contact with ponds (OR, 2.69), treatment of cattle (OR, 2.57), treatment of swine (OR, 1.94), and treatment of wildlife (OR, 1.67) (table 4).

Table 4
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Table 4

Final multivariable model for risk factors associated with seropositivity to Coxiella burnetii among participating veterinarians.

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Discussion

The concept of human, animal, and ecosystem health as “one health” is gaining momentum and may result in further increased emphasis on zoonoses. Few systematic studies have been conducted to ascertain the prevalence of zoonotic infections among veterinary workers, although numerous cases of zoonotic infections have been reported. We found a seroprevalence for C. burnetii of 22.2% among veterinarians attending the AVMA GHLIT Wellness Booth in 2006; this rate is greater than the seroprevalence of 13.3% in 1956, 3.6% in 1966, and 0% in 1968, 1970, and 1972 reported among veterinarians from Illinois [23]. A few studies have been conducted in other countries with varying results [24-27]. The 2 largest studies conducted revealed seroprevalence rates of 9.5% among 137 Austrian veterinarians tested in 1994 and 13.5% among 267 Japanese veterinarians tested from 1997 through 2000 [24, 26]. Interestingly, a study among veterinarians in Nova Scotia demonstrated a seroprevalence rate of 49% among 65 veterinarians, and their multivariate analysis revealed that veterinarians who were male and those who were exposed to sheep placentas were at highest risk [25]. A meta-analysis by McQuiston and Childs [3] reported a seroprevalence for C. burnetii of 7.8% among individuals in the United States who had contact with livestock, including veterinarians, farmers, slaughterhouse workers, and tannery workers.

Anderson et al. [28] used data and serum samples from the 2003–2004 National Health and Nutrition Examination Surveys to estimate the prevalence of antibodies to C. burnetii in the United States [29]. They determined the weighted prevalence for persons aged >20 years in the United States to be 3.07%. The prevalence rate that we detected among veterinarians far exceeds the prevalence rate in the general adult US population; the difference is likely attributable to the difference in the opportunity for exposure to C. burnetii.

Because we collected a single serum sample from participants, we were only able to determine prior exposure to C. burnetii. If we had collected an additional serum sample from participants 2-4 weeks after the first sample, then we may have been able to identify active infections. Additionally, the population of veterinarians attending the AVMA conference may not be representative of all veterinarians in the United States.

Our finding that older veterinarians (aged ⩾46 years) were more likely to have antibodies to C. burnetii is consistent with having had a greater opportunity for exposure during their lifetime [30]. Additionally, the association of seropositivity to C. burnetii with the treatment of cattle, swine, and wildlife is expected, because these animals may serve as reservoirs for C. burnetii [3, 14].

We found that veterinarians who reported frequent contact with water, especially pond water, were more likely to have evidence of exposure to C. burnetii. It has been suggested that when given a choice, female livestock may seek low-lying areas in which to give birth (B. Myers, personal communication). Ponds are often found in such low-lying areas. The shedding of C. burnetii is greatest during parturition and often results in contamination of the environment [14, 31, 32]. Burganskii et al. [33] described an outbreak of Q fever in the Urals in 1955 and raised the possibility of infection with C. burnetii from bathing in and drinking Tobel river water, which was known to be the source of water for herds of cows [34, 35]. In 1959, Welsh et al. [5] found evidence of C. burnetii in 6 (32%) of 19 water samples obtained from pools of standing water in the lambing areas on ranches in Solano County, California. They continued to recover C. burnetii from 2 of the 6 pools of water for 1 month after the initial testing; whether this was because of persistence in the water environment or from repeated contamination was not determined. In another study, from 1980, Yadav and Sethi [36] recovered C. burnetii from 1 of 12 pond-water samples obtained from 3 different ponds. They hypothesized that pond water may contain excrement from infected animals. In vitro, both low (1×10-6) and high (1×10-3) concentrations of C. burnetii can survive for >100 days in tap water at 18°C-22°C and for >140 days at 4°C [37]. In addition, in 2001 La Scola and Raoult [38] detected C. burnetii in the vacuoles of Acanthamoeba castellanii (amoebae) when the 2 organisms were cocultured in vitro. They concluded that the survival of C. burnetii in the environment may be enhanced by their association with free-living amoebae. The soil surrounding bodies of water may also be contaminated, and the inhalation of dust and aerosols from this environment may serve as a route of transmission.

Future outbreak investigations should consider asking questions about water exposure and should be conducted concurrently with an environmental investigation. In addition, veterinarians should wear appropriate personal protective equipment, including a lab coat or equivalent and a mask, when treating animals potentially infected with C. burnetii and especially during assisted births or the handling of birth products of animals known to be carriers of C. burnetii. Although a vaccine against C. burnetii has been developed for use in humans, it is not available in the United States [39, 40]. Because acute Q fever may present with symptoms of influenza-like illness or with evidence of unexplained pneumonia or hepatitis, physicians treating ill veterinarians and others with occupational exposures should consider C. burnetii to be a differential diagnosis. In addition, veterinarians should consider undergoing routine serologic evaluation. Among individuals with underlying heart disease (i.e., with cardiac valve defects or prosthetic valves), receiving immunosupressive therapy (i.e., organ transplant recipients or patients with cancer, lymphoma, chronic renal insufficiency, or HIV infection or AIDS), or who are pregnant, it is essential to diagnose endocarditis due to C. burnetii in the early stages, to prevent complications [14].

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Acknowledgments

We thank Amanda Loftis and Rachael Priestley, for their laboratory assistance, and Jennifer McQuiston, for her thoughtful insights on this study.

Financial support. The O. Wayne Rollins Foundation (grant to the Center for Public Health Preparedness and Research, Rollins School of Public Health, Emory University).

Potential conflicts of interest. All authors: no conflicts.

  • Received September 4, 2008.
  • Accepted October 21, 2008.
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  1. Clin Infect Dis. (2009) 48 (5): 550-557. doi: 10.1086/596705
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