BioMed Research International

BioMed Research International / 2016 / Article

Research Article | Open Access

Volume 2016 |Article ID 7059196 | 7 pages | https://doi.org/10.1155/2016/7059196

Coxiella burnetii Seroprevalence and Risk Factors in Cattle Farmers and Farm Residents in Three Northeastern Provinces and Inner Mongolia Autonomous Region, China

Academic Editor: Daniele Corsaro
Received21 Sep 2015
Revised29 Dec 2015
Accepted10 Jan 2016
Published04 Feb 2016

Abstract

Little is known about Coxiella burnetii infection among cattle farmers and farm residents in China. Thus, the present study was conducted to detect the seroprevalence of C. burnetii infection and estimate associated risk factors among cattle farmers and farm residents in China. A cross-sectional study was designed, and sera of 362 people living or working on 106 cattle farms were tested for C. burnetii IgG and IgM antibodies by immunofluorescence assay. Overall C. burnetii seroprevalence was 35.6% (129/362, 95% CI: 30.70–40.57), and 112 participants had experienced a past infection and seventeen (4.7%) had experienced a relatively recent infection. In the final combined multilevel model, the following activities were significantly associated with presence of antibodies against C. burnetii: milking cattle, providing general healthcare to cattle, providing birth assistance, contact dead-born animals, urbanization, and presence of mice and/or rats in the stable. Moreover, presence of disinfection equipment was a significant protective factor. This is the first study addressing the seroprevalence and risk factors of C. burnetii infection in cattle farmers and farm residents in three northeastern provinces and Inner Mongolia Autonomous Region, China.

1. Introduction

Q fever, caused by Coxiella burnetii (C. burnetii), is a ubiquitous zoonotic disease. Cattle, sheep, and goats are considered as the primary animal reservoirs for human infection. C. burnetii are shed in particularly high concentrations in placentas and birth fluids of infected animals, which may subsequently contaminate the stable environment [1]. Human get infections with C. burnetii mostly by inhalation of contaminated aerosols coming from parturient animals and their birth products [24]. Clinical symptoms of acute Q fever usually present as a self-limited febrile illness, hepatitis, or pneumonia, with very little proportion evolving into chronic infections [57].

Q fever has outbroken in people in some countries, including Spain [8], Switzerland [9], Great Britain [10], Germany [11], and Netherlands [12]. Infections are usual occupational risk in persons working with livestock and contacting with highly infectious aerosols from birth products, milk, urine, faeces, or semen of infected animals [13]. These occupational risk populations include workers in slaughterhouses, meat-packing plants, and tanneries as well as veterinarians and farmers [13]. In China, infection has been detected in humans as well as in a wide range of wild, domestic, and farmed animals such as cattle, goats, dogs, pigs, mice, sheep, and horses [14]. In the previous study, we reported the seroprevalence of C. burnetii infection in farmed ruminants including cattle in the three northeastern provinces and Inner Mongolia Autonomous Region, China [15]. However, information on the seroprevalence and risk factors for acquisition of C. burnetii infection in cattle farmers and farm residents is limited. Thus, the aim of the present study was to determine the seroprevalence in farmers and household members living and/or working on cattle farms and to assess the farm-related and individual risk factors for seropositivity in order to update control measures and to provide targeted advice for this occupational group and the China cattle industry.

2. Materials and Method

2.1. Study Population and Data Collection

This study was approved by the Animal Ethics Committee of Jilin Agriculture University, China. All cattle farms in three northeastern provinces and Inner Mongolia Autonomous Region with at least 50 cattle that were not vaccinated for Q-fever were selected from the register in the census of the zone. As an important cattle and sheep breeding base in China, with the development of economy, farms with different sizes were settled up quickly in Inner Mongolia Autonomous Region. The three northeastern provinces (Jilin, Liaoning, and Heilongjiang provinces) are comprehensive agricultural bases. Poultry, pigs, cattle, sheep, and deer are the main breeding animals in these areas. On eligible farms, we approached cattle farmers and one or two of their household members aged 12 years and older, and in some cases, other persons working or living on the farm such as farm employees. A maximum of five participants were included per farm. Nonresponders received a reminder 3 weeks after the initial invitation. After providing informed consent on farm and individual level, all participating farms were visited by professional laboratory assistants, who collected sera from October 2013 through July 2014. Each participant completed a questionnaire about personal characteristics (e.g., age, medical history, farm-related activities, contact with livestock and companion animals, and use of personal protective equipment). The farm owner or manager completed a questionnaire about herd size, cattle housing, presence of other livestock and companion animals, farm facilities, and hygiene measures.

2.2. Serological Method

An immunofluorescence assay (IFA) (Focus Diagnostics, Cypress, CA, USA) was used to test serum samples for C. burnetii phases I and II IgM and IgG. All samples were screened at an initial dilution of 1 : 32; those with negative results were considered negative. Positive samples were further classified as indicative of relatively recent infections (IgM phase II titer >32) or past infections (IgG phase II titer >32 and IgM phase II titer <32). Samples with all other outcomes were considered negative. The term relatively recent was chosen because phase II IgM is commonly found up to 1 year after infection in acute Q fever cases, but it may persist up to 3 years [16]. Phases I and II IgG end point titers were determined for all seropositive persons. In agreement with chronic Q fever diagnostic criteria used in the Netherlands [17], phase I IgG titers ≥1,024 in samples in the past infection group were considered indicative of possible chronic infection.

2.3. Statistical Analysis

Results were analyzed with SPSS 19.0 software package. For comparison of the frequencies among the groups, the Mantel-Haenszel test and when indicated the Fisher exact test were used. Bivariate, multivariate, and multilevel analyses were used to assess the association between participant- and farm-based characteristics of the subjects and the C. burnetii infection. Variables were included in the multivariate analysis if they had a value of equal or less than 0.20 in the bivariate analysis. Adjusted odd ratio (OR) and 95% confidence interval were calculated by multivariate analysis using multiple, unconditional, and logistic regression. A value less than 0.05 was considered statistically significant.

3. Results

3.1. Descriptive Characteristics

Of all 197 invited eligible cattle farms, 106 (53.8%) farms participated in this study. The number of cattle farms from Heilongjiang, Jilin, Liaoning, and Inner Mongolia was 21, 28, 22, and 35, respectively. The mean herd size was 95 cattle (range 50–327) in participating farms. From the 106 participating farms, 362 persons provided a blood sample (mean age 46.0 years (12–68), 45.3% male) (Table 1). All of the farm-based and participant-based questionnaires were completed by the 106 farmers and 362 persons.


VariableCategoryFreq. ()Seroprevalence (%)95% CI

Participant 36235.64 30.70–40.57

SexMale19836.36 29.66–43.06
Female16434.76 27.47–42.04

Age group<355635.71 23.16–48.26
35–447830.77 20.53–41.01
45–5413738.69 30.53–46.84
≥559135.17 25.35–44.98

FunctionFarmer19338.34 31.48–45.20
Spouse8931.46 21.81–41.11
Child4531.11 17.59–44.64
Other3537.14 21.14–53.15

RegionHeilongjiang9830.61 21.49–39.74
Jilin7627.63 17.58–37.69
Liaoning9231.52 22.03–41.02
Inner Mongolia9651.04 41.04–61.04

represents other family members and employees.
3.2. Seroprevalence of C. burnetii

Overall C. burnetii seroprevalence was 35.6% (129/362, 95% CI: 30.70–40.57), and seroprevalence among farmers, spouses, children, and others was 38.3%, 31.5%, 31.1%, and 37.1%, respectively (Table 1). Of the 129 seropositive participants, 112 participants had experienced a past infection and seventeen (4.7%) had experienced a relatively recent infection, as demonstrated by presence of IgM phase II antibodies. IgG phase II end titers were known for the 76 participants with a past infection with IgG phase I <1 : 32: 1 : 32 (), 1 : 64 (), 1 : 128 (), 1 : 256 (), 1 : 512 (), and ≥1 : 1024 (). For the 36 participants with a past infection with IgG phase I ≥1 : 32, 3 persons had “possible chronic Q fever” with IgG phase I titers ≥1 : 1024 according to diagnostic standard used in the Netherlands [8]. We could not confirm that these truly were chronic Q fever cases due to lack of clinical information (e.g., presence of vascular infection, endocardial involvement, or other clinical risk factors).

3.3. Risk Factors for C. burnetii Infection

All individual and farm-based variables, which were tested in the bivariate analysis for relationship with human C. burnetii seropositivity, are shown in Tables 2 and 3.


VariableCategoryFreq. ()Seroprevalence (%)OR (95% CI) value

Work and/or live on farmWork and live24540.41 2.03 (0.98–4.22)0.023
Work, but not live7326.03 1.06 (0.45–2.49)
Not working, but live4425.00 Reference

Hours working on farmFulltime17437.36 1.32 (0.65–2.66) 0.853
Halftime10935.78 1.23 (0.59–2.59)
Quarter week3432.35 1.06 (0.41–2.76)
Sometimes/never4531.11 Reference

How often in stableEvery day18938.62 1.39 (0.70–2.79) 0.426
Every week10435.58 1.22 (0.58–2.58)
Every month3828.95 0.90 (0.35–2.32)
Less than once a month/never3125.81 Reference

Feeding cattleYes29938.45 2.19 (1.16–4.14)0.014
No6322.22 Reference

Milking cattleYes20343.84 2.32 (1.48–3.65)<0.001
No15925.16 Reference

General healthcare of cattleYes24142.32 2.56 (1.55–4.21)<0.001
No12122.31 Reference

Remove manureYes28635.66 1.01 (0.59–1.71)0.982
No7635.53 Reference

Spread manureYes25840.31 2.13 (1.28–3.57)0.002
No10424.04 Reference

Clean stablesYes26939.03 1.84 (1.09–3.11)0.022
No9325.81 Reference

Birth assistanceYes21642.59 2.19 (1.38–3.46)<0.001
No14625.34 Reference

AdministrationYes21938.81 1.43 (0.91–2.23)0.076
No14330.77 Reference

Wear overalls or bootsYes23338.63 1.45 (0.92–2.30)0.110
No12930.23 Reference

Having a dogYes29435.03 0.87 (0.51–1.50)0.619
No6838.24 Reference

Having a catYes27835.25 0.93 (0.56–1.55)0.782
No8436.90 Reference

Direct contact with cattle in their own or other farmsYes28738.68 2.00 (1.12–3.57)0.018
No7524.00 Reference

Direct contact with horses in their own or other farmsYes21039.52 2.56 (1.61–4.07)<0.001
No15223.68 Reference

Contact with raw milkYes24343.21 3.01 (1.80–5.04)<0.001
No11920.17 Reference

Contact with cattle manureYes22544.00 2.80 (1.73–4.54)<0.001
No13721.90 Reference

Contact with dead-born animalsYes19645.41 2.62 (1.67–4.12)<0.001
No16624.10 Reference

Contact with placenta/birth materialYes18838.30 1.27 (0.83–1.96)0.272
No17432.76 Reference


VariableCategoryNumber of humans testedPositive (%)OR (95% CI) value

RegionHeilongjiang9830.61 Reference
Jilin7627.63 0.87 (0.45–1.68)0.667
Liaoning9231.52 1.04 (0.56–1.93)0.892
Inner Mongolia9651.04 2.36 (1.31–4.25)0.004

UrbanizationModerate or minor urban area149 20.81Reference<0.001
Rural area213 46.013.24 (2.01–5.24)

Herd sizeSmall (50–100) 197 32.48Reference0.393
Medium (100–150)104 39.421.35 (0.83–2.22)
Large (>150)61 39.341.35 (0.74–2.44)

Beef cattle on the farmYes202 37.131.16 (0.75–1.79)0.505
No160 33.75Reference

Number of stables>3 stables117 32.480.81 (0.51–1.30)0.386
≤3 stables245 37.14Reference

Use of artificial inseminationYes84 46.431.81 (1.10–2.98)0.018
No278 32.37Reference

Laying hens on farmYes243 40.331.92 (1.18–3.11)0.008
No119 26.05Reference

Presence of cat(s) in cattle stablePresent198 36.361.07 (0.70–1.65)0.751
Absent164 34.76Reference

Use of silageYes276 40.222.54 (1.43–4.51)0.001
No86 20.93Reference

Use of maizeYes288 38.191.79 (1.01–3.17)0.045
No74 25.68Reference

Feeding methodFodder mixer or automatic241 32.370.66 (0.42–1.03)0.067
Hand/wheelbarrow121 42.15Reference

Presence of mice and/or rats in the stablePresent199 45.232.63 (1.67–4.14)<0.001
Absent163 23.93Reference

Farm visitorsYes143 37.761.17 (0.75–1.81)0.495
No219 34.25Reference

Farm boots for staffYes277 36.461.17 (0.70–1.95)0.553
No85 32.94Reference

Presence of hygienic locker roomYes269 31.970.55 (0.34–0.88)0.013
No93 46.24Reference

Presence of disinfection equipmentYes224 29.460.50 (0.32–0.77)0.002
No138 45.65Reference

Birds in stableYes90 45.561.75 (1.08–2.85)0.023
No272 32.35Reference

Veterinary serviceYes301 31.621.40 (0.78–2.54)0.273
No61 29.51Reference

Type of farm managementClosed herd298 34.890.84 (0.48–1.46)0.528
Purchase of cattle64 39.06Reference

In the multivariate analyses, from 14 individual variables which were associated in the bivariate analysis, six were independently associated with C. burnetii seropositivity (Table 4). Moreover, 5/18 farm-based variables included in the multilevel analyses were significantly independent risk or protective factors and together were used as the full multilevel start model (Table 5).


VariableCategoryAdjusted odds ratio95% confidence interval value

Milking cattleYes1.881.21–2.940.005
NoReference

General healthcare of cattleYes2.401.46–3.93<0.001
NoReference

Birth assistanceYes2.071.31–3.270.002
NoReference

Contact raw milkYes2.471.50–4.06<0.001
NoReference

Contact cattle manureYes3.231.92–5.44<0.001
NoReference

Contact dead-born animalsYes3.452.16–5.50<0.001
NoReference

The variables included were those with a obtained in the bivariate analysis.
Adjusted by age and the rest of characteristics included in this table.

VariableCategoryAdjusted odds ratio95% confidence interval value

UrbanizationRural area3.662.25–5.96<0.001
Moderate or minor urban areaReference

Laying hens on farmYes2.041.25–3.320.004
NoReference

Use of silageYes1.991.15–3.440.013
NoReference

Presence of mice and/or rats in the stablePresent2.491.58–3.91<0.001
AbsentReference

Presence of disinfection equipmentYes0.580.37–0.900.015
NoReference

The variables included were those with a obtained in the bivariate analysis.
Adjusted by age and the rest of characteristics included in this table.

In the final combined multilevel model, significant risk factors were milking cattle, general healthcare of cattle, birth assistance, contact dead-born animals, urbanization, and presence of mice and/or rats in the stable. Moreover, presence of disinfection equipment was a significant protective factor (Table 6).


VariableCategoryAdjusted odds ratio95% confidence interval value

Milking cattleYes2.091.33–3.270.001
NoReference

General healthcare of cattleYes2.251.38–3.670.001
NoReference

Birth assistanceYes1.861.18–2.920.005
NoReference

Contact dead-born animalsYes2.671.69–4.45<0.001
NoReference

UrbanizationRural area2.341.41–3.45<0.001
Moderate or minor urban areaReference

Presence of mice and/or rats in the stablePresent1.951.38–3.010.002
AbsentReference

Presence of disinfection equipmentYes0.370.20–0.49<0.001
NoReference

The variables included were those with a obtained in the bivariate analysis.
Adjusted by age and the rest of characteristics included in this table.

4. Discussion

This is the first study exploring the seroprevalence in cattle farmers and farm residents in China, and one of few risk factor studies on human C. burnetii infections in farm populations worldwide [1820], suggesting that living and or working on cattle farm has a high lifetime risk for acquiring C. burnetii infection. Farmers and other household members are usually at highest risk for acquiring C. burnetii infection due to close contact with infected cattle and contaminated stables on farms.

The detected seroprevalence was high not only for the farmers (38.3%), as expected, but also among spouses (31.5%), children (31.1%), and others (37.1%) who lived and often also worked at the farm. The present seroprevalence obviously overs the estimates of 10.2% in the people studied to date in China [14]. The seroprevalence was also lower than those in other studies focusing on, nonfurther specified, farm populations, such as 49% among farmers from Northern Ireland [21], 72.1% in dairy cattle farmers in the Netherlands [18], but was comparable to the 27% seroprevalence in a farm cohort in the United Kingdom [10]. However, it is complicated to compare these seroprevalences due to some differences, including geographical conditions, the different study populations, diagnostic methods, and living styles. Moreover, in the present study, females have a higher seroprevalence than males. It is contrary to other places in the world where studies have suggested that males are more susceptible to C. burnetii infection [2]. Routine activities of women in rural areas including taking care of livestock and cleaning stables result in the high prevalence in females in China [14].

Several independent individual and farm-based risk factors for C. burnetii seropositivity were found such as working and/or living in farm, milking cattle, general healthcare of cattle, birth assistance, contacting raw milk, contacting cattle manure, contacting dead-born animals, urbanization, laying hens on farm, use of silage, presence of mice and/or rats in the stable, presence of disinfection equipment, and birds in stable. The individual risk factor involving direct contact with cattle or dust-producing activities in the cattle stable, such as milking, general healthcare of cattle, clean stables, birth assistance, contacting raw milk, contacting cattle manure, and contacting dead-born animals, reflects the stable environment contact [22]. Under these circumstances the risk of inhalation of contaminated aerosols is high, with a potential increased risk for acquiring an infection. The degree of total farm animal contact has been reported to seem more important than particular animal exposure, suggesting that risk of C. burnetii exposure is largely connected with farm environment contact [6, 22].

Two farm-related risk factors were identified to be associated with human seropositivity among cattle farm residents/staff: urbanization and presence of mice and/or rats in the stable. The concentration and management of cattle farming in the rural area of the study regions possibly promoted transmission between farms. The presence of mice and/or rats in the stable was observed as risk factor for human seropositivity, suggesting C. burnetii introduction or facilitation of spread by infected wild animals [2325]. Moreover, presence of disinfection equipment was observed as protective factor for human seropositivity.

It is worth noting that Q fever is out of notifiable diseases in China and thus it is not easy to get test facilities. Most cases are diagnosed through retrospective and epidemiological studies which implies that misdiagnosis often occurred for acute cases, resulting in the greater possibility of chronic infections which have a poor prognosis and high mortality [14]. Thus, routine serological follow-up is helpful for prevention as well as basic biological safety rules, such as hygiene measures and the use of protection clothes.

To conclude, high C. burnetii seroprevalences demonstrate that cattle farmers and farm residents have a substantial lifetime risk for acquiring this zoonotic infection. We recommend reinforcing routine biosecurity measures to avoid indirect spread, avoiding access of companion and wild animals to the stable, and offer advice on eliminating nuisance animals in the cattle stables. Clinicians should strengthen their awareness to consider Q fever in this occupational group presenting with compatible symptoms or relevant sequelae to allow diagnosis and therapy in time.

Conflict of Interests

The authors declare that there is no conflict of interests in this paper.

Acknowledgment

Project support was provided by the project National Natural Science Foundation of China (Grant no. 31272566).

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Copyright © 2016 Wu-Wen Sun et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


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