Transmission and control of Fish-borne Zoonotic Trematodes in aquaculture

150 Pages·2013·2.45 MB·English

by  Boerlage, Annette

Transmission and control of
Fish-borne Zoonotic Trematodes
in aquaculture

Annette S. Boerlage
Thesis committee

Promotors
Prof. dr. ir. M.C.M. de Jong
Professor of Quantitative Veterinary Epidemiology
Wageningen University

Prof. dr. J.A.J. Verreth
Professor of Aquaculture and Fisheries
Wageningen University

Co-promotor
Dr. ir. E.A.M. Graat
Assistant professor, Quantitative Veterinary Epidemiology Group
Wageningen University

Other members
Prof. dr. ir. I.J.M. de Boer, Wageningen University
Prof. dr. I.A. Gardner, University of Prince Edward Island, Charlottetown,
Canada
Prof. dr. ir. W. Takken, Wageningen University
Dr. M.E.E. Kretzschmar, University Medical Center (UMC) Utrecht and
National Institute for Public Health and the Environment (RIVM),
Bilthoven

This research was conducted under the auspices of the Graduate School

of Wageningen Institute of Animal Sciences (WIAS).
Transmission and control of
Fish-borne Zoonotic Trematodes
in aquaculture

Annette S. Boerlage

Thesis
submitted in fulfilment of the requirements for the degree of doctor
at Wageningen University
by the authority of the Rector Magnificus
Prof. dr. M.J. Kropff,
in the presence of the
Thesis Committee appointed by the Academic Board
to be defended in public
on Wednesday 3 July 2013
at 11 a.m. in the Aula.
Annette S. Boerlage

Transmission and control of Fish-borne Zoonotic Trematodes in
aquaculture, 150 pages.

PhD thesis, Wageningen University, Wageningen, NL (2013)
With references, with summaries in English and Dutch

ISBN: 978-94-6173-628-4
ABSTRACT

Boerlage, A.S. (2013). Transmission and control of Fish-borne Zoonotic
Trematodes in aquaculture. PhD Thesis, Wageningen University,
Wageningen, The Netherlands.

Fish-borne Zoonotic Trematodes (FZTs) affect the health of millions of
humans worldwide. For persistence, the life cycle of FZTs depends on
aquatic snails, fish, and definitive hosts like humans, pigs or chickens.
Definitive hosts can become infected by eating raw or undercooked fish.
Integrated Agriculture Aquaculture (IAA) systems improve the livelihood
of small scale farmers, but may enhance transmission of FZTs because
all types of hosts and all transmission routes can be present on a single
farm. This thesis combines experiments, statistical analyses and
mathematical modelling to gain insight into transmission mechanisms of
FZTs to fish in aquaculture and to use this insight to compare and
discuss control measures against FZTs. Currently, medication of humans
is the main strategy to control FZTs. Modelling indicated that this does
not lead to elimination of FZTs because both humans and definitive
hosts other than humans will maintain the life cycle of FZTs
independently. Treatment of (a part of) these host types may eliminate
FZTs, e.g. treating all humans and 54% of definitive hosts other than
humans. Aquaculture may provide opportunities for control of FZTs by
adapting management measures. Experiments showed that smaller fish
get more often and more heavily infected with FZTs than larger fish;
common carp (Cyprinus carpio) of more than 50 g rarely acquire new
infections. Once carp are infected, FZTs persist for at least 27 weeks,
implying that harvestable fish still contain FZTs and, therefore, are a risk
to human health. In most IAA systems, fish are kept FZT free until 0.5 g
before being stocked into a fish pond where they are very likely to be
exposed to FZTs. Stocking fish at more than 25 g, or at more than 14 g
in combination with treating all humans with anthelmintics, may lead to
elimination of FZTs. Also, control of snails by either decreasing density
or increasing mortality of snails may lead to elimination of FZTs in
aquaculture. Farmers and policy makers should evaluate which
combination of control measures is attractive to them.

Contents Page

1 General introduction 9

2 Distribution of trematodes in snails in ponds at 21
integrated small-scale aquaculture farms

3 Effect of fish size on transmission of fish-borne 35
trematodes (Heterophyidae) to common carp
(Cyprinus carpio) and implications for intervention

4 Higher attack rate of fish-borne trematodes 49
(Heterophyidae) in common carp fingerlings (Cyprinus
carpio) at lower fish weight

5 Survival of heterophyid metacercariae in common 59
carp (Cyprinus carpio)

6 Transmission of fish-borne trematodes 67
(Heterophyidae) to common carp (Cyprinus carpio) is
independent on fish and trematode density

7 Effect of control strategies on the persistence of fish- 79
borne zoonotic trematodes: a modelling approach

8 General discussion 103

References 113

Summary 127

Samenvatting 133

About the author 139
Curriculum vitae
List of publications
WIAS training and supervision plan
Acknowledgement / dankwoord

Colophon

1

General introduction
Introduction

More than 10% of the human population is at risk of infection with
crustacea-, plant-, or fish-borne zoonotic trematodes. These trematodes
affect the health of more than 40 million people (Abdussalam et al.,
1995; WHO, 2011) and affect economics in terms of loss of productivity,
absenteeism, and health care costs. Furthermore, food safety issues can
affect trade (Roberts et al., 1994; WHO, 1995, 2004).
This thesis focuses on fish-borne zoonotic trematodes (FZTs).
Humans can become infected with FZTs when they consume raw or
undercooked fish. The association between human infections and FZTs in
fish is well described for fisheries, but has been neglected for
aquaculture until about 15 years ago (Lima dos Santos and Howgate,
2011). This is surprising, because 40% of the worldwide production of
fish origins from aquaculture (FAO, 2012). Farmers can manage fish in
aquaculture, which may provide opportunities for control of FZTs. This
thesis combines experiments, statistical analysis and mathematical
modelling of FZT in aquaculture to improve understanding of the impact
of several control measures. This first chapter is an introduction on FZTs
in general, FZTs in Vietnam, FZTs in aquaculture, control measures
against FZTs in humans and control measures against FZTs on
aquaculture farms. It ends with the objective and outline of this thesis.

General

The life cycle of FZTs depends on three types of hosts; primary snail
hosts, secondary fish hosts, and definitive hosts like humans, dogs or
fish-eating birds (Fig. 1).
10