Scientific Opinion on Q fever

EFSA Journal 2010; 8(5):1595 [114 pp.]. doi:10.2903/j.efsa.2010.1595
  EFSA Panel on Animal Health and Welfare Panel Members Panel members AHAW: Anette Bøtner, Donald Broom, Marcus G. Doherr, Mariano Domingo, Jörg Hartung, Linda Keeling, Frank Koenen, Simon More, David Morton, Pascal Oltenacu, Albert Osterhaus, Fulvio Salati, Mo Salman, Moez Sanaa, James M. Sharp, Jan A. Stegeman, Endre Szücs, Hans-H. Thulke, Philippe Vannier, John Webster and Martin Wierup. Panel members BIOHAZ: Olivier Andreoletti, Herbert Budka, Sava Buncic, John D. Collins, John Griffin, Arie Havelaar, James Hope, Günter Klein, Tine Hald, Winy Messens, James McLauchlin, Christine Mueller-Graf, Christophe Nguyen-Thé, Birgit Noerrung, Miguel Prieto Maradona, Luisa Peixe, Antonia Ricci, John Sofos, John Threlfall, Ivar Vågsholm, Emmanuel Vanopdenbosch. Acknowledgment The AHAW Panel wishes to thank the members of the Working Group on Q fever for the preparation of this opinion: Simon More (Chair), Jan Arend Stegeman, Annie Rodolakis, Hendrik-Jan Roest, Piet Vellema, Richard Thiéry, Heinrich Neubauer, Wim van der Hoek, Katharina Staerk, Howard Needham (ECDC) and the EFSA staff members Ana Afonso, Milen Georgiev and Jane Richardson for the support provided to this EFSA scientific output. Thank you also for the valuable information made available by the Zoonoses task force, the EFSA Animal Health and Welfare network, Prof. S. Martinov and I. Yordanov.This opinion was the result of a fruitful collaboration with ECDC in relation to public health aspects. The BIOHAZ Panel wishes to thank the EFSA staff member Bart Goossens for the support provided to Chapter 4 of this EFSA scientific output. Contact ahaw@efsa.europa.eu
Type: Opinion of the Scientific Committee/Scientific Panel On request from: European Commission Question number: EFSA-Q-2010-00010 Adopted: 27 April 2010 Published: 12 May 2010 Affiliation: European Food Safety Authority (EFSA), Parma, Italy
Abstract

Following a request from the European Commission, a scientific opinion was prepared by EFSA’s Animal Health and Welfare Panel to determine the magnitude, distribution, impact and significance of infection and disease in domestic ruminants and humans, risk factors for the maintenance (in domestic ruminant populations) and spillover (from these populations to humans) of Coxiella burnetii (the causative agent of Q fever), and control options in domestic ruminant populations. A range of approaches were used, including an assessment of monitoring/surveillance data, the development of a simple conceptual model, a critical review of available literature, and several country case studies. Control options for C. burnetii infection in small ruminants were qualitatively assessed. Infection is endemic in domestic ruminants in most, if not all, EU member states, however, disease is rare and impact is limited. In the EU, Q fever is a zoonotic disease with limited public health impact, except under certain epidemiological circumstances and for particular risk groups. Human cases are often associated with proximity to small ruminants (particularly at parturition or during abortions) and dry, windy weather. Currently, there is no clear evidence of an association between bacterial genotypes/isolates and virulence. A number of longer-term options to control C. burnetii infection in domestic ruminants were identified; these should be considered in those situations where the public health risk is considered unacceptable. Some additional options were not considered sustainable for long-term control, but may have a role in the face of an outbreak. Persistent environmental contamination may confound animal-based control efforts. Vaccination should be considered a long-term control option, noting that effectiveness may not be observed in the short-term. Antibiotic treatment of animals is not recommended. There is no conclusive evidence that the consumption of milk and milk products containing C. burnetii has resulted in clinical Q fever in humans.

© European Food Safety Authority, 2010

Summary

The recent developments in the EU, especially the increase in confirmed human cases of Q fever in the Netherlands, call for special consideration as regards the risks posed by Q fever for humans and animals. The European Commission requested further scientific advice and risk assessment, as regards Q fever in animals. The mandate posed three questions:

  • to assess the significance of the occurrence of Q fever in the EU Member States for a better understanding of the scale and distribution of the disease and infection (with the focus on farm animals and humans)
  • to assess the risk factors for Q fever occurrence and persistence in animal husbandry and the related risks for humans, and
  • to assess the effectiveness and efficiency of disease control options.

An opinion, in response to the mandate, was prepared by the EFSA Panel on Animal Health and Welfare, with input from EFSA’s Panel on Biological Hazards (BIOHAZ) and the Zoonoses and Assessment Methodologies Unit, and in close collaboration with the European Centre for Disease Prevention and Control (ECDC).

Several approaches were adopted during the preparation of this scientific opinion. An assessment of the magnitude and distribution of infection and disease in domestic ruminants and in humans was conducted after considering diagnostic methods for Coxiella burnetii infection (the causal agent of Q fever) and monitoring/surveillance for C. burnetii infection in different member states of the European Union (MS). Impact and significance was assessed, based on expert opinion. Several methods were used to clarify risk factors for maintenance of C. burnetii infection in domestic ruminants and spillover of infection from domestic ruminants to humans, including the development of a simple conceptual model, a critical review of available literature, and several country case studies. Control options for C. burnetii infection in domestic ruminant populations were evaluated, following the development of a generic framework for the control of infectious diseases, and based on available data about individual control interventions.

Infection with Coxiella burnetii (the causal agent of Q fever) is endemic in domestic ruminants (cattle, sheep, goats) in most, if not all, EU MS. Although infection in domestic ruminants is common, disease is rare. The overall impact of C. burnetii infection on the health of domestic ruminants in EU MS is limited. In humans, C. burnetii infection is present in most, if not all, EU MS. Q fever is a zoonotic disease with limited public health impact in the EU, however, in certain epidemiological circumstances and for particular risk groups the public health impact can be significant. As yet, the Q fever burden of disease in humans has not been determined.

It seems likely that C. burnetii infection can be maintained in domestic ruminants in a wide range of husbandry systems. There is considerable uncertainty about the relative importance of risk factors for maintenance of C. burnetii infection in domestic ruminant populations, and for spillover from domestic ruminants to humans. Nonetheless, maintenance of C. burnetii infection within farms might be favoured by persistently infected animals, other animal reservoirs of infection, ticks, husbandry practices that favour within-herd transmission and/or environmental contamination. Currently, there is no clear evidence of an association between bacterial genotypes/isolates and virulence. The common risk factors associated with spillover of infection from domestic ruminants to humans in different EU MS include an association between human infection and small ruminants (sheep and goats), an indication of proximity between animals and human populations, particularly in association with parturition in animals (and to abortions, in the case of goats), and specific climatic conditions, in particular dry, windy weather. In humans, the risk of exposure to C. burnetii is increased, either following close contact to animals infected with C. burnetii, or following community-based exposure (caused by an elevation of C. burnetii in the wider environment following release and dissemination from infected animal hosts). There is no conclusive evidence in support of a link between an increased density of animals and/or farms and spillover of C. burnetii from infected farms to humans. The factors leading to outbreaks of Q fever in the human population are not fully understood.

Regarding disease control, the opinion focused on control options applicable to domestic ruminants, and on the effectiveness of these options to reduce within-herd transmission, between-herd spread (each in domestic ruminant populations), and/or the spillover of infection from domestic ruminants to humans. For almost all of the control options, there is a medium to high level of uncertainty associated with estimates of control effectiveness, as little relevant published information is available. It is likely that control methods would need to be used in combination. There is variation in the sustainability of the assessed control options. A number of long-term control options were identified, including preventive vaccination, manure management, changes to farm characteristics, wool shearing management, a segregated lambing/kidding area, removal of risk material, visitor ban, control of other animal reservoirs and tick control. All but the latter two relate specifically to small ruminants. These options are ranked according to effectiveness, as assessed by expert opinion, in reducing spillover from domestic ruminants to humans. Several options were not considered sustainable for long-term control, but may have a role in the face of an outbreak, including the culling of pregnant animals, a temporary breeding ban, stamping out, identification and culling of shedders, control of animal movements and stand still. These options all relate specifically to small ruminants. C. burnetii is highly resistant in the environment; consequently, persistent environmental contamination is a matter of concern. Vaccination can be used both to reduce the risk of future outbreaks (preventive vaccination) and in the face of an outbreak (outbreak vaccination), noting that preventive vaccination is more effective than outbreak vaccination, phase I is more effective than phase II vaccination, vaccination is more effective in non-infected than infected animals, vaccination does not appear to be effective if used in pregnant females, and effectiveness may not be observed in the short-term.

The Animal Health and Welfare Panel recommended harmonized field and laboratory data collection about C. burnetii infection in animals in EU MS, to allow comparison of prevalence/incidence estimates over time and between countries. Further, there is a need to strengthen systems to promote rapid identification and reporting of Q fever outbreaks in animals (abortion episodes). Consideration should be given for support of early information exchange between veterinarians and public health counterparts regarding potential events with zoonotic potential, including Q fever. Further studies on the estimation of Q fever burden of disease in humans are needed. Prevalence and incidence studies in domestic ruminants should place emphasis on small ruminants, rather than cattle, to provide a clearer picture of the risk of exposure for humans. Further investigations and research are needed to clarify the relationship between genotype and virulence, the molecular basis for virulence, and the relationship between mice models and virulence studies in domestic ruminants, determine the host specificity of different bacterial isolates, identify factors influencing the maintenance of infection, including an improved understanding of transmission pathways, quantify the number of bacteria excreted under different conditions, quantify survival of C. burnetii in the environment, clarify the role of environmental contamination and climatic factors in the spillover of infection from animals to humans, and clarify the trade off between farm density and farm size in the maintenance and spillover of infection. Future investigations are needed to objectively assess the effectiveness of control options for C. burnetii infection in domestic ruminant populations. Assessment should focus on relevant epidemiological parameters, including rates of within-herd transmission, between-herd spread and spillover from animal populations to humans. Control options should generally be used in combination, given that within-herd transmission, between-herd spread and spillover to humans are each likely to involve more than one transmission pathway, and that no control option is likely to be completely effective in limiting within-herd transmission, between-herd spread and spillover to humans. Longer-term options to control C. burnetii infection in domestic ruminants should be considered in those situations where the public health risk is considered unacceptable. Control options where effectiveness at reducing spillover was assessed as either high or medium include preventive vaccination, appropriate manure management, changes to farm characteristics, wool shearing management, segregated lambing/kidding area, removal of risk material and visitor ban. Control options to address proximity between humans and small ruminants, particularly around the time of lambing/kidding, would be expected to meaningfully contribute to a reduction in spillover from animal populations to humans. There is a need to build awareness among farmers and veterinarians of C. burnetii infection in farmed ruminants, including risk factors for spillover from domestic ruminant populations to humans. Short term options such as the culling of pregnant animals, a temporary breeding ban, stamping out, identification and culling of shedders, control of animal movements and stand still could be used to reduce shedding from infected animals. However, other options (including preventive vaccination, manure management, wool shearing management, segregated lambing/kidding area, removal of risk material) should be considered to reduce human exposure through environmental contamination. Vaccination should be considered as a long-term control option. In order to better assess vaccine efficacy, it is recommended that field and experimental data are gathered, to improve our understanding of the epidemiology of C. burnetii infection in, and between, infected flocks, both prior to and following vaccination. Antibiotic treatment is not effective in substantially reducing either the level or duration of bacterial shedding in domestic ruminant populations; therefore the use of antibiotics cannot be recommended.

The widespread distribution of C. burnetii in food producing animals and its occurrence in the milk supply necessitates questioning the role of food as a vehicle for the transmission of this zoonotic bacterium to humans. C. burnetii infection in occupationally or otherwise exposed people is mainly due to inhalation of infected aerosols rather than consumption of contaminated food (e.g. dairy, meat) products. However, C. burnetii is excreted in milk of infected animals (cattle, sheep and goats) for variable periods during lactation irrespective whether these animals are showing clinical signs or not and in addition, milk can be contaminated with C. burnetii by faecal materials or from sites of infection in the periparturient and/or lactating animal. Consumption of raw milk and raw milk products represent a relatively greater risk of human exposure to C. burnetii than the consumption of both milk and dairy products made with milk that has undergone appropriate heat treatment. There are epidemiological indications that consumption of milk and/or milk products containing C. burnetii has been associated with sero-conversion in humans. However, there is no conclusive evidence that the consumption of milk and milk products containing C. burnetii has resulted in clinical Q fever in humans.

The scientific opinion was adopted by the Scientific Panel on Animal Health and Welfare (AHAW) on 27 April 2010. Chapter 4 (focusing on food safety issues) and related conclusions were adopted by the Scientific Panel on Biological Hazards (BIOHAZ) on 22 April 2010.
 

Keywords

Q fever, EU, Coxiella burnetii, domestic ruminants, public health, risk factors, control options