Elsevier

Vaccine

Volume 35, Issue 46, 1 November 2017, Pages 6283-6289
Vaccine

Changing livestock vaccination policy alters the epidemiology of human anthrax, Georgia, 2000–2013

https://doi.org/10.1016/j.vaccine.2017.09.081 Get rights and content

Abstract

Anthrax is a widely spread zoonotic disease found on nearly every continent. To control the disease in humans and animals, annual livestock vaccination is recommended. However, in 2007, the country of Georgia ended its policy of compulsory annual livestock anthrax vaccination. Our objective was to assess how the epidemiology of human anthrax has evolved from 2000–2013 in Georgia, in the wake of this cessation. We used passive surveillance data on epidemiological surveys of human anthrax case patients. Risk factors and rates of self-reported sources of infection were compared, before and after the change in livestock vaccination policy. We mapped ethnicity-adjusted incidence during the two periods and assessed changes in the spatial pattern of risk. The overall risk of human anthrax increased >5-fold, from 0.7 cases per 100,000 in 2000 to 3.7 cases per 100,000 by 2013. Ethnic disparities in risk became pronounced; from 2000 to 2013, incidence increased >60-fold in Azerbaijanis from 0.35 to 21.1 cases/100,000 Azerbaijanis compared to 0.61 to 1.9 cases/100,000 among ethnic Georgians. Food-borne exposures from purchasing meat increased from 11% in 2000–2006 to 21% in 2007–2013. Spatial analyses revealed a shift from a random pattern of reporting pre-policy change to clustering among district municipalities following the change in policy. Our findings indicate there were unintended human health consequences associated with changing livestock vaccination policy. Following a reduction in the immunizations administered, there was a major shift in the epidemiology of human anthrax in Georgia. Current infection risk is now highest among ethnic minorities. Increased reporting among individuals uncharacteristically at risk for anthrax from foodborne exposures suggests spillover from modes of agricultural production. Given the importance of human-livestock health linkages, careful evaluations of policy need to be undertaken before changes to animal vaccination are made.

Introduction

Anthrax is a zoonotic disease that is found on nearly every continent (except Antarctica) [1], [2]. The causative agent, Bacillus anthracis, is a soil-borne Gram-positive bacterium with the remarkable ability to survive in the environment for long periods of time, perhaps years, and infect a wide range of hosts [2], [3]. Herbivorous animals are most often infected [2], [3], [4]. Human infections are typically a result of contact with infected animals or their by-products (e.g. meat or hides) during activities such as livestock slaughtering [1], [4].

Targeting livestock with annual vaccination is the most effective method to control anthrax in both humans and animals in endemic regions [1], [5]. The most widely used vaccine is the live attenuated Sterne strain (34F2) [5]. In the former Soviet Union (FSU), livestock anthrax vaccination combined with improvements in occupational safety produced a nearly 10-fold reduction in animal cases with a concomitant decline in human incidence [6]. Similar decreases were observed in Europe and the United States following mass vaccination of livestock [7]. However, despite the effectiveness of vaccination, anthrax persists in areas with weakened health infrastructures and long-term vaccination strategies may be needed in endemic areas [1], [8]. Countries of the FSU, sub-Saharan Africa, and southeast Asia have (re)emerged as foci for transmission [9].

The country of Georgia has experienced repeated outbreaks of human anthrax with a recent increase in human incidence (2010–2012) [10]. Reports of an anthrax-like disease in humans dates to the 17th century [11] and >500 locations have been registered as foci (permanent locations of anthrax risk) in Georgia since 1881 [12]. During Soviet governance, anthrax was a mandatory reportable infectious disease in both humans and livestock. Following the dissolution of the Soviet Union in 1991, and Georgian independence in December of the same year, anthrax reporting remained mandatory. To combat the spread of anthrax, from 1995 through 2006, the government carried out annual compulsory livestock vaccination. In 2007, Georgia ended this policy, placing the responsibility of vaccination on private livestock owners [13].

Yet, little is known about how the alteration in livestock immunization policy and the concomitant decline in the number of anthrax vaccine doses administered affected the epidemiology of human anthrax. In the context of >90% private livestock ownership in Georgia, and the high risk associated with agricultural production, identifying changes in anthrax epidemiology are crucial for implementing control strategies and limiting its spread. Our objective was to assess how the change in livestock vaccination policy impacted the epidemiologic characteristics of human anthrax in Georgia from 2000–2013 by identifying changes in risk factors and rates of self-reported sources of infection.

Section snippets

Methods

We obtained passive surveillance data on epidemiological surveys of human anthrax case patients and the annual number of livestock vaccine doses administered from the National Centers for Disease Control and Public Health (NCDC) during 2000–2013. We estimated national incidence rates per 100,000, using population data from the Georgian national census (Georgian State Statistical Committee, GeoStat). To describe the trend in human anthrax incidence and identify trend breakpoints if present, we

Temporal trends

From 2000 to 2013, 736 human anthrax cases (annual range: 15–143) were reported in Georgia (Fig. 1). During this 14-year period, the trend in rates was characterized by a breakpoint in the regression line in the year 2010 (95% CI: 2008, 2011) indicating an increasing rate of reporting post-policy change with an AAPC = 10.2% (95% CI: 9.3, 10.9; p = .02) (Fig. 1). The annual human incidence per 100,000 increased from 0.6 cases (95% CI: 0.4, 0.8) in 2000 to 3.7 cases (95% CI: 3.1, 4.4) in 2013.

Discussion

During Soviet governance (1950–1980), the incidence of human anthrax declined, in part, due to widespread livestock vaccination mirrored by reductions worldwide [5], [6], [7], [9], [19]. However, in endemic areas, long-term livestock vaccination may not be tenable due to costs and there is a paucity of evidence regarding the impact of cessation policies [9]. Our findings show that following changes to livestock vaccination policy in Georgia, which reduced immunizations administered, there was a

Conclusion

The change in livestock vaccination policy has dramatically affected the epidemiology of human anthrax in Georgia. In addition to the increasing rates of transmission, the epidemiology of the disease has shifted such that ethnic enclaves, and in particular, Azerbaijanis, are now at highest risk. Furthermore, the likely spillover of contaminated meat and animal by-products from agriculture into markets has increased the frequency of infections among occupations uncharacteristically at risk for

References (31)

  • I. Kracalik et al.

    Human cutaneous anthrax, Georgia 2010–2012

    Emerg Infect Dis

    (2014)
  • P. Imnadze et al.

    Anthrax in southern Caucasus

    Antibiot Monit

    (2002)
  • Kukhalashvili T. Anthrax foci in Georgia;...
  • A. Navdarashvili et al.

    Human anthrax outbreak associated with livestock exposure: Georgia, 2012

    Epidemiol Infect

    (2016)
  • H. Kim et al.

    Permutation tests for joinpoint regression with applications to cancer rates

    Stat Med

    (2000)
  • Cited by (0)

    View full text