Downloaded from http://oem.bmj.com/ on December 23, 2014 - Published by group.bmj.com

OEM Online First, published on December 17, 2014 as 10.1136/oemed-2014-102457 Exposure assessment

ORIGINAL ARTICLE

Risk factors for new infection with Leptospira in meat workers in New Zealand A Dreyfus,1,2 P Wilson,3 J Collins-Emerson,4 J Benschop,4 S Moore,4 C Heuer1 ▸ Additional material is published online only. To view please visit the journal online (http://dx.doi.org/10.1136/ oemed-2014-102457). 1

EpiCentre, Institute of Veterinary, Animal and Biomedical Science, Massey University, Palmerston North, New Zealand 2 Section of Epidemiology, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland 3 Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand 4 mEpiLab, Infectious Disease Research Centre (IDReC), Hopkirk Research Institute, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand Correspondence to A Dreyfus, Section of Epidemiology, Vetsuisse Faculty, University of Zurich, Winterthurerstrasse 270, Zurich 8057, Switzerland; [email protected] Received 15 July 2014 Revised 20 October 2014 Accepted 1 December 2014

ABSTRACT Objective To evaluate risk factors for new infection with Leptospira interrogans sv Pomona and Leptospira borgpetersenii sv Hardjo in meat workers. Methods Sera were collected twice approximately 12 months apart from 592 workers from eight abattoirs slaughtering sheep, cattle or deer and tested by microscopic agglutination for Pomona and Hardjo. Information on potential risk factors were recorded and analysed by multivariable logistic regression. Results Forty-nine (8.3%) participants, either seroconverted or had at least a titre increase by two dilutions against either serovar. While in sheep meat workers, the annual infection risk was 11.3% (95% CI 8.5% to 14.8%), in deer meat workers it was 0% (95% CI 0.0% to 10.9%) and in those processing beef cattle, 1.2% (95% CI 0.2% to 4.6%). Risk factors for new infection in sheep abattoirs were worker position, abattoir and time worked in the meat industry. The new infection risk was highest at the beginning of the slaughter line (stunning and hide removal; relative risk, RR 7.5, 95% CI 2.5 to 22.4), followed by positions on the line involving the removal of high-risk material (bladder, and kidneys; RR 5.2, 95% CI 1.7 to 16.0). Risk was lower in the offal/pet food area (RR 4.1, 95% CI 1.0 to 16.4), and lowest in the boning room or office. Wearing personal protective equipment did not reduce the risk of new infection. Conclusions This study has demonstrated ongoing exposure to leptospires in meat workers and risk factors for challenge. We recommend measures such as improvement of personal protective equipment use, changes in slaughter procedure or vaccination of sheep against Leptospira to reduce the risk.

INTRODUCTION

To cite: Dreyfus A, Wilson P, Collins-Emerson J, et al. Occup Environ Med Published Online First: [please include Day Month Year] doi:10.1136/oemed2014-102457

Leptospirosis is a zoonotic bacterial disease with a worldwide distribution, and is achieving increased recognition. It is especially endemic in subtropical and tropical countries, but is also prevalent in many countries with pastoral livestock industries. Incidence in people is generally under-reported due to lack of awareness of the disease and of surveillance and because of complexity of diagnosis.1 2 Transmission occurs from exposure to urine or aborted tissues of infected animals, either directly or via contact with contaminated water or soil.3 Human leptospirosis is more common in occupationally exposed groups such as farmers (livestock or rice paddy fields), butchers or abattoir workers, forestry workers, miners, sewer workers, veterinarians or military personnel.2

What this paper adds ▸ Abattoir workers and people in agro-forestry occupations are at risk for contracting leptospirosis in New Zealand. Risk factors for infection with Leptospira interrogans sv Pomona and Leptospira borgpetersenii sv Hardjo in abattoirs and the incidence of new infections were unknown and required for developing control measures. ▸ This cohort study demonstrated that there was a substantial risk of infection with the two Leptospira serovars studied, especially at sheep abattoirs, and that the risk of exposure was highest at the beginning of the slaughter process, where stunning and pelting occurs. ▸ It also raised questions about ‘best practice’ use of personal protective equipment, since wearing gloves, facemasks and goggles were not protective factors in the multifactorial risk model. ▸ To protect workers, meat processing industries should consider alterations to the slaughter procedure or vaccination of livestock a prerequisite for slaughter.

New Zealand (NZ) has a relatively high incidence of notified human leptospirosis cases among temperate developed countries4 and a medium position for the Asia Pacific region5 with an average annual rate of 2 cases per 100 000 population.6 In NZ, livestock are the main source of human leptospirosis, with farmers and meat workers being most at risk.4 The two most frequent serovars in cattle, deer and sheep in NZ are Leptospira borgpetersenii sv Hardjo (Hardjo) and Leptospira interrogans sv Pomona (Pomona).7–9 Studies revealed that 62% of farmed deer8 and 5.7% lambs sampled in abattoirs were seropositive against Hardjo and/or Pomona.10 Based on culture, an abattoir worker was exposed to 5–26 lamb carcasses shedding Leptospira per day, hence presenting many opportunities for human infection.11 Whereas almost all dairy farmers vaccinate their stock against leptospirosis and the NZ pig industry has introduced compulsory vaccination of herds,12 less than 10% of deer, sheep or beef farmers are currently using vaccination for leptospirosis.13 14 In the past four decades, four cross-sectional studies investigated Leptospira seroprevalence in meat workers in NZ15–18 estimating seroprevalences against Pomona, Hardjo, and/or Leptospira borgpetersenii sv Tarassovi of between 4.1% and 31%. In an

Dreyfus A, et al. Occup Environ Med 2014;0:1–7. doi:10.1136/oemed-2014-102457

Copyright Article author (or their employer) 2014. Produced by BMJ Publishing Group Ltd under licence.

1

Downloaded from http://oem.bmj.com/ on December 23, 2014 - Published by group.bmj.com

Exposure assessment abattoir processing sheep, workers on the slaughter board had, depending on their work position, a 23–85-fold higher risk of being seropositive than workers in the boning, cutting, chilling or rendering areas.19 However, no longitudinal study investigating risk factors for Leptospira incidence risk in abattoirs has been conducted. The objective of this study was therefore to identify risk factors for new infection with Leptospira related to occupational as well as non-occupational activities in meat workers. The findings were likely to generate recommendations for the improvement of control measures in abattoirs. The work in this article formed part of the PhD thesis of the main author and was submitted in January 2013 to the Institute of Veterinary, Animal and Biomedical Sciences at Massey University, Palmerston North, New Zealand.19a

METHODS Study design, data collection and management We conducted a cohort study among voluntarily participating meat workers from eight purposively selected abattoirs comprising four sheep (one (‘sheep 1’) studied twice and three studied once), two beef and two deer abattoirs in NZ. The two deer abattoirs were located in the South Island and the sheep and beef abattoirs were in the North Island. To estimate the risk of new infection with Leptospira, sample and data collection occurred twice at intervals ranging from 50 to 61 weeks. Participating meat workers were blood sampled by certified phlebotomists and interviewed at each blood sampling by trained researchers using a questionnaire (see online supplementary material). The first blood sample was used to establish the initial antibody titre status against Pomona and Hardjo and the second determined whether or not a worker was infected during the study period.

Sample size estimation To detect a relative risk (RR) of 2.5 for new infections, assuming a prevalence of a risk factor of 10% in the unexposed population, to achieve 80% power and 95% confidence, 280 meat workers had to be sampled twice. The number was doubled to consider clustering due to sampling at several abattoirs.20

Serological testing The microscopic agglutination test (MAT) was used to measure serum antibodies against Pomona and Hardjo at doubling dilutions from 1:24 to 1:1536 as described previously.21 The MAT was always performed by the same trained laboratory technician. To measure seropositivity, a titre cut-off of ≥1:48 was used to declare that a worker was previously exposed to leptospires.21 22 Seroconversion occurred where a seronegative worker (120–216 >216 ≤84 >84–198 >198–324 >324 No Yes Don’t know/maybe Sheep 1§ Sheep 1 Sheep 2 Sheep 3 Sheep 4

37 11.5 22.9 28.7 27.3 7.6 4.7 60.4 36.5 6.8 3.4 53.4 83.3 16.7 73.4 26.6 17.2 16.4 13.8 52.6 28.1 21.9 26.3 23.7 73.3 25.2 1.5 21.4 35.2 17.7 5.5 20.3

2.8 9.1 14.8 23.6 9.5 3.4 22.2 13.8 8.6 7.7 7.7 15.6 12.2 12.5 11.7 13.7 9.1 17.5 11.3 11.9 5.6 14.3 7.9 23.1 13.4 11.5 20.0 13.4 9.6 17.6 14.3 10.3

Ref 3.2 5.2 8.4 Ref 0.4 2.3 1.4 Ref 0.9 0.9 1.8 Ref 1.0 Ref 1.2 Ref 1.9 1.2 1.3 Ref 2.6 1.4 4.2 Ref 0.9 1.5 Ref 0.7 1.3 1.1 0.8

Wear gloves on both hands

Wear goggles/glasses

Wear a facemask Wear a balaclava Months worked at current abattoir*

Months worked in meat industry

Urine splashed in face†

Abattoir

(142) (44) (88) (110) (105) (29) (18) (232) (140) (26) (13) (205) (320) (64) (282) (102) (66) (63) (53) (202) (108) (84) (101) (91) (253) (87) (5) (82) (135) (68) (21) (78)

95% CI

p Value

(0.8 to 12.9) (1.7 to 16.1) (2.9 to 24)

0.098 0.004 40, ≤50 >50, ≤57.5 >57.5 No Yes No Yes NZ European NZ Maori Other No Yes

33.3 (128) 66.7 (256) 25.8 (99) 25.0 (96) 24.2 (93) 25.0 (96) 92.5 (355) 7.6 (29) 83.9 (322) 16.2 (62) 42.7 (164) 49.2 (189) 8.1 (31) 83.3 (320) 16.7 (64)

7.8 14.5 10.1 9.4 16.1 13.5 12.1 13.8 12.7 9.7 9.1 14.8 12.9 12.5 10.9

Ref 1.9 Ref 0.9 1.6 1.3 Ref 1.1 Ref 0.8 Ref 1.6 1.4 Ref 0.9

Age (years)

Hunting pigs, deer or feral goats Farming* Ethnicity

Slaughtering at home†

95% CI

p Value

(0.9 to 3.7)

0.084

(0.4 to 2.3) (0.7 to 3.6) (0.6 to 3.1)

0.871 0.252 0.486

(0.4 to 3.2)

0.804

(0.3 to 1.8)

0.53

(0.9 to 3.0) (0.5 to 4.3)

0.132 0.541

(0.4 to 2.0)

0.744

*Pigs, goats, sheep, beef cattle, alpaca or deer. †Sheep, goats, pigs, beef or deer. NZ, New Zealand.

Dreyfus A, et al. Occup Environ Med 2014;0:1–7. doi:10.1136/oemed-2014-102457

3

Downloaded from http://oem.bmj.com/ on December 23, 2014 - Published by group.bmj.com

Exposure assessment cumulative incidence was multiplied by 36 515. CIs were calculated by the Fleiss method.24 For sheep abattoir workers, the new infection risk was shown for each exposure variable described in tables 1 and 2. Crude associations between the risk of infection with Hardjo and/or Pomona and putative risk factors or confounding factors listed in tables 1 and 2 were calculated for sheep abattoir workers by bivariable and multivariable logistic regression (LR). A forward stepwise selection method with a Wald/χ2 test p value of 0.3 as an entry criterion was chosen to evaluate risk factors and confounding variables in the multivariable model, starting with a null model with only an intercept included and then adding one risk factor at a time. A risk factor was retained if the likelihood ratio test (LRT) was statistically significant at a p value ≤0.05 or if its presence changed the crude coefficient of the work position (the main effect variable) and/or fitted risk factor variables in the model by ±15%. Interaction between risk factors was tested by multivariable LR. If the LRT was statistically significant ( p≤0.05) the interaction term was retained in the model. The tested interaction terms were ‘gender*wearing gloves’, ‘work position*gender’, ‘work position*wearing gloves’, ‘work position*wearing safety/ normal glasses’, ‘wearing gloves*abattoir’ and ‘wearing safety/ normal glasses*abattoir’. Since the risk period was very similar for workers in all plants and each participant had been followed through the risk period, the RR was used for the interpretation of risk factors. A Poisson model with a log-link was used for calculating RR as described by McNutt et al.25 Since 57 people from abattoir ‘Sheep 1’ participated twice in the study, over-dispersion was estimated to decide whether adjustment for clustering due to repeated measurements was required in the analysis. Over-dispersion was declared present if the ratio between the residual Pearson χ2 and residual degrees of freedom was greater than 1.5.26 In that case, robust SEs were calculated using generalised estimating equations realised in ‘proc genmod’ of SAS where the participant was abattoir. We tested the assumption of linearity for the continuous risk factor variables. The Hosmer-Lemeshow statistic was used to test the distributional assumption and the pseudo-R2 was used to evaluate the overall model fit. Influential covariate patterns and leverage were examined using described methods.27

RESULTS The number of workers by abattoir ranged from 21 to 135 (sheep), 58 to 100 (beef ) and 18 to 32 (deer) with a total of 384 sheep, 50 deer and 158 beef abattoir workers participating.

The seroprevalence against Hardjo and/or Pomona measured at the first sampling was on average 13% in sheep, 17% in deer and 5% in beef abattoir workers. At the second sampling, approximately a year later, prevalence was 18% (sheep), 15% (deer) and 6% (beef ). These estimates were not significantly different between years. The frequency of workers wearing PPE differed by species and abattoir (p≤0.001). Whereas in sheep abattoirs 70% (range 47– 81% between abattoirs) of slaughter board, yard and offal room workers reported wearing gloves on both hands (always or often), 4% (range 0–8%) of workers did in deer and 88% (range 84–94%) in beef abattoirs. Seventy-three per cent of sheep (range 10–88% between abattoirs), 52% of deer (range 31–80%) and 29% (range 20–43%) of beef slaughter board, yard and offal room workers reported wearing safety/normal glasses and 26%, 9% and 0%, respectively, wore facemasks (always or often). There were also statistically significant differences for the use of PPE in specific work positions across sheep abattoirs. While 89% of persons working in the stunning area of sheep abattoir 1 reported wearing glasses, 12% did in sheep abattoir 3 (p324 1(S1), 3,4,1(S2)* 2

Ref 4.1 5.2 7.5 Ref 3.0 1.3 3.0 Ref 2.0

Months worked in the meat industry

Abattoir

95% CI

p Value

(1.0 to 16.4) (1.7 to 16.0) (2.5 to 22.4)

0.048 0.004

Risk factors for new infection with Leptospira in meat workers in New Zealand.

To evaluate risk factors for new infection with Leptospira interrogans sv Pomona and Leptospira borgpetersenii sv Hardjo in meat workers...
214KB Sizes 0 Downloads 4 Views