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Field evaluation of targeted selective treatments to control subclinical gastrointestinal nematode infections on small ruminant farms
Accepted Manuscript Title: FIELD EVALUATION OF TARGETED SELECTIVE TREATMENTS TO CONTROL SUBCLINICAL GASTROINTESTINAL NEMATODE INFECTIONS ON SMALL RUMINANT FARMS Author: F. Valc´arcel A. Aguilar M. S´anchez PII: DOI: Reference:
S0304-4017(15)00204-6 http://dx.doi.org/doi:10.1016/j.vetpar.2015.04.014 VETPAR 7606
To appear in:
Veterinary Parasitology
Received date: Revised date: Accepted date:
14-7-2014 10-4-2015 20-4-2015
Please cite this article as: Valc´arcel, F., Aguilar, A.,FIELD EVALUATION OF TARGETED SELECTIVE TREATMENTS TO CONTROL SUBCLINICAL GASTROINTESTINAL NEMATODE INFECTIONS ON SMALL RUMINANT FARMS, Veterinary Parasitology (2015), http://dx.doi.org/10.1016/j.vetpar.2015.04.014 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
*Highlights (for review)
FIELD EVALUATION OF TARGETED SELECTIVE TREATMENTS TO CONTROL SUBCLINICAL GASTROINTESTINAL NEMATODE INFECTIONS IN SMALL RUMINANT FARMS Hightlights
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We model three TST programs under five management types of small ruminants Performance and healthy status are good after TST application Regular anthelmintic dosage could not be necessary in subclinical nematodosis TST are more useful when a minimum of nematode burden is present in the farms
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*Revised Manuscript with NO changes marked (clean)
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TITLE
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FIELD EVALUATION OF TARGETED SELECTIVE TREATMENTS TO
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CONTROL SUBCLINICAL GASTROINTESTINAL NEMATODE INFECTIONS
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ON SMALL RUMINANT FARMS.
AUTHORS
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Valcárcel, F.; Aguilar, A.; Sánchez, M.
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POSTAL ADDRESSES
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Félix Valcárcel, [email protected]
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Ana Aguilar, [email protected]
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María Sánchez, [email protected]
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Grupo de Parasitología Animal, Centro de Investigación en Sanidad Animal
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(INIA-CISA), 28130 Valdeolmos (Madrid), Spain.
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CORRESPONDENCE ADDRESS
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Félix Valcárcel Sancho DVM, PhD
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Parasitology Group, Animal Health Research Center (INIA-CISA) 28130
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Valdeolmos (Madrid), Spain
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Tel.: 0034 91 620 23 00
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Fax: 0034 91 620 22 47
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E-mail address: [email protected]
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ABSTRACT
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Targeted selective treatments (TST) are designed to identify those
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animals that would actually benefit from anthelmintic treatment, thus reducing
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the amount of drugs used and bringing down economic cost. In this study we
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assayed three TST programs based on GIN egg output, clinical sign and live
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weight criteria in a single area where only sub-clinical infections tend to occur
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and no Anthelmintic Resistance is reported. The study was carried out from
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February 2011 to August 2013 on four farms applying different management
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systems: an Ovine Extensive System, Ovine Semi-extensive Semi-irrigated
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System focusing on “Rubia del Molar” and Colmenareña” breeds, Ovine Semi-
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extensive System and Caprine Organic Semi-extensive System.
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The number of sheep and goats treated in all the TST strategies was
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lower in comparison with systematic treatments, especially when selected
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based on clinical signs (100%, in both years), followed by egg output (87.57%
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and 90.44% in the first and second year respectively) and finally by live weight
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(37.95% and 96.69%, in the first and second year respectively). FEC was low
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throughout the study for all animals and groups. Apparently, the TST applied did
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not influence live body weight.
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Preliminary results show that all three targeted selective treatments
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significantly reduced the number of animals treated and the cost of anthelmintic
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treatment on the farms, maintaining productivity in a low challenge environment.
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These results also seem to indicate that systematic anthelmintic treatments are
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unnecessary under these circumstances and traditional anthelmintic regimes
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should therefore be modified.
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KEY WORDS
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Subclinical gastrointestinal nematodosis, targeted selective treatments,
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extensive management systems, small ruminants.
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1. INTRODUCTION
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Like many other agricultural production sectors, sheep husbandry is
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strongly influenced by environmental changes brought about by global climate
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change. Climate change can lead to the emergence of new diseases or
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changes in the prevalence of existing ones (Summers, 2009; Kenyon et al.,
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2009a). In this context, gastrointestinal nematodes (GIN) still remain a serious
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threat to small ruminant farming worldwide (Bentounsi et al., 2012; Mederos et
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al., 2012). Control of parasitic infections should be based on both knowledge of
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its
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pharmacological products. However, most livestock producers administer
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anthelmintic treatment without any supporting diagnostic or epidemiological
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knowledge (Kenyon and Jackson, 2012; Valcárcel et al., 2013).
appropriate
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While intensive or suppressive chemical treatment strategies can give
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rise to maximum production rates, they may not be economically sustainable
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and could lead to anthelmintic resistance (AR). Furthermore, AR is the single
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most important factor hindering the control of nematode parasite infection on
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small ruminant farms (Gilleard, 2006) and is global (for a review, see Jabbar et
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al., 2006). Therefore, a reduction in drug use is desirable to fight AR where it
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exists and to prevent unnecessary spending on small ruminant farms. The aim
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of targeted selective treatment (TST) is to identify those animals that could truly
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benefit from anthelmintic treatment thus reducing the use of drugs and
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economic cost. TST programs must be designed for each specific area and
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treatment application indicators need to be selected carefully (Greer et al.,
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2009). The objective is to apply the best criteria to animal selection which
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depends on the epidemiology of the parasites and the management system
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employed (Rinaldi and Cringoli, 2012); effective application depends on the
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accurate identification of those animals in need of anthelmintic treatment
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(Bentounsi et al., 2012). TST programs have been successfully applied in areas where clinical
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signs are evident and/or where AR has developed (Gallidis et al., 2009; Cringoli
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et al., 2009; Ouzir et al., 2011; Kenyon et al., 2013). However, it is not clear
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whether they work well in areas where GIN mainly produce subclinical
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infections as is the case on many small ruminant farms in Europe (Kenyon and
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Jackson, 2011; Valcárcel et al., 2013b). In this study we evaluated three TST
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programs based on GIN egg output, clinical signs or body weight loss in one
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area where only subclinical infections occur and no AR is reported.
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2. MATERIALS AND METHODS
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2.1.
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Sampling area and study farms
The study was conducted from February 2011 to August 2013 in the
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central part of the Iberian Peninsula. According to the Köppen-Geiger
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classification (Essenwanger, 2001; AEMET, 2011), the climate in this area is
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Mediterranean with Continental and Atlantic influences, characterized by cold
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winters and warm summers.
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Four farms applying different management systems were selected for the
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study (two in the province of Cuenca and two in the province of Madrid). On one
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of the Madrid farms, two breeds were managed and were considered separately
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(flocks 2 and 3). So, briefly, the study was performed in five flocks: Ovine
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Extensive System; Ovine Semi-extensive Semi-irrigated System featuring the
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“Rubia del Molar” breed; Ovine Semi-extensive Semi-irrigated System featuring
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the “Colmenareña” breed; Ovine Semi-extensive System and Caprine Organic
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Semi-extensive System (Flocks 1 to 5, respectively). Sampling started in
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different months depending on when the study animals were born. Details about
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farm characteristics and management are shown in Table 1. Study groups and sampling
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Between 51 and 64 animals per farm, depending on availability, were selected
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for the study.
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The condition of the animals was assessed at the beginning of the study. They
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were weighed, individually examined by a veterinary and a fecal sample was
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taken to evaluate GIN egg output. Selected animals from each farm were
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distributed in three balanced groups following three TST criteria in terms of
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body weight and faecal egg counts (FEC). All TSTs criteria were performed on
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all the farms
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Once selected, animals were tested every month throughout the duration of the
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study (11 to 24 months depending on the farm). This included weighing, an
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external veterinary inspection to detect clinical signs and the taking of individual
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fecal samples to estimate FEC determined by means of a modified salt-
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floatation technique with a saline solution (1.18 specific gravity) sensitive to one
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egg per gram of feces (epg) (Jackson, 1974 and modified by Kenyon et al.,
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2013).
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The animals put in the three groups were managed just like the general flock
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except for the anthelmintic treatment regime: Egg Output Group (EOG), in
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which animals were treated individually only when elimination was equal or
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higher than 300 GIN eggs per gram of feces (epg); Clinical Sign Group (CSG),
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in which animals were individually treated only when clinical signs were
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observed (diarrhea, severe bodyweight loss or anemia); and Live Weight Group
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(LWG), in which animals were individually treated only when bodyweight was
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lower than 90% of the average weight of this group.
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All anthelmintic treatments administered throughout the study consisted of
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albendazole (Valbazen® 28%CO, 5 mg per kg live weight). The dose was
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determined according to body weight measured on the day of testing. Animals
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that met the deworming criteria for two consecutive months were only given the
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anthelmintic treatment at first detection.
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No other anthelmintic treatments were administered during the study.
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2.2.
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Parasites were identified as per Valcárcel et al. (2013a).
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2.3.
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The following parameters were measured when comparing study groups:
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monthly live bodyweight; monthly, annual and global FEC; monthly, annual and
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global cumulative FEC; clinical signs; and number of times animals were
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dewormed. Differences between groups (p=0.05 or p<0.01) were estimated by
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t-Student test.
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1. Differences in FEC among Flocks and anthelmintic treatment regimes
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In order to study differences in FEC among Flocks and anthelmintic treatment
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regimes, a factorial-ANOVA was tested, employing average FEC in the first
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year as a dependent variable and the flock and treatment as factors. Scheffé’s
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test was used as a post-hoc analysis.
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established for this analysis.
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Parasite identification
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Data analysis.
A confidence interval of 99% was
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2. Saving of the different anthelmintic treatment regimes in the first year
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A Wilcoxon matched paired test was carried out to determine whether there
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were significant differences between the theoretical number of treatments and
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the number of treatments performed on each flock- anthelmintic treatment
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regime group.
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Two Kruskal-Wallis tests were performed to compare treatment savings among
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flocks and among anthelmintic treatment regimes. Treatment savings are
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defined as the percent reduction in the number of treatments actually performed
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compared to the theoretical number of treatments. These were calculated for
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each anthelmintic treatment regime and for each flock. A multiple comparisons
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of mean ranks test was used as a post-Hoc test. A confidence interval of 95%
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was established for these analyses.
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3. RESULTS
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3.1. Anthelmintic usage
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The number of sheep and goats treated in accordance with TST strategies was
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reduced compared with systematic treatments, especially where treatment was
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based on the clinical signs criterion (100%, in both years) followed by egg
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output (87.57% and 90.44% respectively for year one and two) and finally by
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live weight (37.95% and 96.69% respectively).
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The number of treatments performed was lower than the theoretical number for
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all anthelmintic treatment groups (Table 2). The Wilcoxon matched pairs test
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identified significant differences between the number of theoretical treatments
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and ones actually performed in each group (W=0; p<0.05). As a consequence,
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savings from fewer treatments were statistically significant. In addition, there
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were no significant differences in the number of treatments among flocks (H4=1,
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p>0.05), but important differences were found among treatment regimes
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(H2=10.44; p<0.05; Figure 6). The multiple comparisons test showed that there
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were significant differences between the EOG anthelmintic treatment regime
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and the CSG regime. LWG was between these two.
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3.1.1. Egg Output anthelmintic treatment.
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Reduction in deworming frequency based on Egg Output was quite
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variable, ranging from 48.53% to 100% in year one and from 75% to 100%
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in year two (Table 2).
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A total of 19 anthelmintic treatments were administered to the EOG in year
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one, most of them in flock 1 (14 treatments), followed by flocks 3 (4
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treatments) and 2 (1 treatment). No anthelmintic treatments were needed
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for the EOG in flocks 4 and 5.
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The number of treatments administered from month 13 forward declined
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significantly in the three flocks tested for periods longer than twelve months
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(1 to 3); only five treatments were necessary (four in flock 3 and one in flock
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1).
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3.1.2. Live Weight anthelmintic regime.
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The reduction in the number of times animals were dewormed based on the live
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weight criterion was also very variable among the different flocks, especially in
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year one ranging from 12.50% in flock 3 to 77.94% in flock 1.
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The reduction was similar for the three flocks checked in year two (flocks 1, 2
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and 3; 96.32%, 100% and 93.75%, respectively). A total of 72 and 35
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treatments were needed in the first and second years respectively. These
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treatments were distributed throughout the year in all of the flocks.
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3.1.3. Clinical Signs determining anthelmintic treatment.
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The clinical signs observed were cough, nasal mucus discharge, ticks
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presence (Hyalomma lusitanicum and Rhipicephalus bursa) and lesions in
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oral mucosa (the latter only observed in animals from flocks 2 and 3 due to
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a brief herbage quality) either CSG, LWG or EOG. None of the animals
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exhibited clinical signs warranting deworming.
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Therefore, reduction in annual anthelmintic treatment based on CSG was
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100% for all the flocks.
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3.2. Animal performance
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TST did not appear to influence live bodyweight which was similar in the three
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study groups in all the flocks (Figures 1.I and 2.I).
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We only observed slight isolated differences in live bodyweight between LWG
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and CSG in flock 1 from February to May during the second year (p=0.05).
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No differences in live bodyweight were found between study groups in the other
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flocks.
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3.3. Parasitological results
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3.3.1. GIN pattern
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Through the salt-floatation analysis we regularly observed Trichostrongylidae,
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Nematodirus, Trichuris and Moniezia eggs; Dictyocaulus and protostrongilid first
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stage larvae; and Eimeria oocysts.
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FEC were consistently low throughout the study in all flocks and groups
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(Figures 1.II and 2.II) with a maximum of 275 epg in flock 1. Despite this low
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level, in year one FEC in flocks 1 to 3 exhibited a bimodal pattern with a peak
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three months after starting to graze and a second peak five-six months later.
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FEC was much lower as from month 13.
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FEC in flocks 4 and 5 was very low but a small increase was observed five and
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four months respectively after starting to graze.
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3.3.2. Application of TST
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Factorial ANOVA showed that there were no significant global differences
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among treatments (F(2,199)=0.92; p>0.05), but important difference were
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observed among flocks (F(4,199)=114.21; p<0.05; (Figure 5)). Scheffé’s test
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identified three homogenous groups, flock 1 2 being the two flocks with higher
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average FEC values, flock 2 had an intermediate mean value and flocks 4 and
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5 were the two flocks with the lowest average FEC.
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In flock 1, the mean FEC was higher (95.21 epg) when the Clinical Signs
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criterion was applied, followed by Egg Output and lastly by Live Weight. These
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differences with EOG (81.46 epg) and LWG (78.28 epg) were very significant
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(p<0.01) during the first year (Figure 3.I). Either from month 13 forward (Figure
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3.II) and during the entire study (Figure 3.III), we only observed weak
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differences between CSG and LWG (87.90 epg; 59.64 epg, p=0.05).
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In contrast, FEC in CSG in the other flocks was lower than in EOG and LWG
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but the differences were not significant.
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Similarly, we only observed weak differences (p=0.05) in cumulative FEC
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between CSG and LWG in flock 1 during the first year (1,039.85 epg, 671.04
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epg, Figure 4.I) and during the entire study (1,467.96 epg and 994.16 epg,
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Figure 4.III).
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Monthly FEC and cumulative FEC of the “Colmenareña” breed (flock 3) (Figure
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1.II) were significantly higher than in “Rubia del Molar” (flock 2) (Figure 1.III)
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(p<0.01) as from month two and most of the following months up to the end of
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the study (Figure 1.II and 1.III).
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The results of fecal egg count reduction test (FECRT) in other animals from
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flocks 1 to 3 seem to indicate that there was no presence of AR development
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(data not shown).
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FEC was very low throughout the study, especially during the second year, and
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was systematically lower following the administration of Live Weight and Egg
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Output anthelmintic treatments than after the Clinical Sign regime. These
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results suggest a much lower worm burden than that reported in the area at the
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end of the XXth century for both domestic and wild ruminant species (García-
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Romero et al., 1993; Valcárcel and García Romero, 1999; Valcárcel et al.,
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2002). Despite this fact, farmers continue applying the same anthelmintic
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strategies and today small ruminants in the area receive 1.6 anthelmintic doses
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per year specifically to control GIN (Valcárcel et al., 2013b). This indicates that
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farmers are slow to assimilate change as is the case in other parts of Europe
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(Jackson et al., 2009).
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No treatment was administered to any of the animals in the CSG group from all
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the flocks and they maintained low FEC, animal performance and health status,
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suggesting a very low worm burden. Similarly, despite the fact that animals from
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the LWG group required a greater number of treatments, they did not exhibit
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any clinical signs of GIN infection or high egg output. Smaller animals frequently
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met the criteria for several consecutive months warranting deworming. Finally,
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the results obtained for the EOG group are somewhere in the middle between
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the other two.
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FEC does not always reflect the current nematode burden (van Wyk et al.,
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2006) but Egg Output does appear to be an accurate way of identifying animals
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affected by worms (Gallidis et al., 2009). Theoretically, this appears to be the
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most reasonable criterion because only those animals exhibiting a pre-defined
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egg elimination rate are treated. However, it is more expensive because
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requires a greater degree of animal management, regular coprological
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analyses, etc.
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Under the study’s subclinical infection conditions, these criteria did not appear
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to be useful in selecting animals for deworming. However, it is important to note
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that presumably only a small number of animals actually needed anthelmintic
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treatment. The results from flock 1, the only one that reached a minimum
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elimination rate during the study, seem to support this idea and better results
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would be expected in areas with a higher nematode burden as previously
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reported (Greer et al., 2009; Bentounsi et al., 2012; Kenyon et al., 2009b,
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2013). Other authors reported that the Live Weight criterion is very useful in
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identifying animals in need of treatment in areas where the worm burden is
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large enough to produce either severe production loss or disease (Greer et al.,
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2009, 2010; Stafford et al., 2009, Bentounsi et al., 2012) because there is
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evidence to support the hypothesis that both of them are produced by GIN.
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TST based on a health indicator (daily weight gains) and an infection indicator
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(number of eggs per gram of feces) can, in one grazing season, successfully
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control anthelmintic resistance and the negative effects of nematode infections
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(Gaba et al., 2010) and is more readily accepted by farmers needing help in
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organizing TST (Berrag et al., 2009). The success of these approaches will
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depend on the extra profit realized by producers (Kahn and Woodgate, 2012).
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The benefits of a TST program only will be seen where there is a minimum
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worm burden on the farm. It may be difficult to get farmers to accept a TST
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program in areas where only sub-clinical infections tend to occur and/or AR
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goes unreported. TST programs require more management procedures and the
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reduction in the cost of anthelmintic treatments must financially offset the
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economic cost of coprological analysis and management. Therefore, we need to
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change the way we deliver worm control messages, properly expressing the
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reasons to change, invisible pain, innovators and other factors (Woodgate and
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Love, 2012).
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With a view to improving the TST approach and making it more applicable
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under practical farming conditions, the advantages of automated weighing
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systems could be considered (van Wyk et al., 2006; Busin et al., 2014). A few
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extra animals are likely to be treated unnecessarily but this will do no great
307
harm to the TST principle (Bath and van Wyk, 2009). In areas where GIN
308
infections are sub-clinical, a combination of criteria that are easy to apply and
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acceptable by farmers would probably be most useful in targeting animals for
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deworming; e.g. selecting only those that fulfilled the three criteria for
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deworming and testing only during the spring and autumn seasons.
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Due the low level of elimination of Nematodirus eggs along the study it was not
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possible to extract a conclusion about this genus. However, other parasites as
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ticks or Protostrongylid nematodes could be important targets of parasite control
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strategies in the area. We aware that salt-floatation technique with 1.18 specific
316
gravity is not a suitable technique to detect Protostrongylids; but the
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appearance of L1 stages by this technique as well abundant nasal mucous
318
discharge during cold months could indicate that we should pay attention on
319
them. We also should consider the possible presence of Oestrus ovis, very
320
often in the area (Martínez-Valladares et al., 2013), as cause of this nasal
321
discharge. Unfortunately we could not perform necropsies to confirm that. In the
322
same way, we cannot be sure about the presence or absence of AR because,
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when FECRT was performed, egg elimination were below the recommended
324
threshold for FECRT to be reliable (Coles et al., 2006).
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CONCLUSION
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The preliminary results of this study in a low challenge environment show that
328
all three of the selection criteria significantly reduced the number of animals
329
treated and the cost of anthelmintic treatment maintaining productivity without
330
any disturbance of health status or production capacity. Furthermore, these
331
results also appear to indicate that systematic anthelmintic treatments are not
332
necessary under these circumstances and traditional anthelmintic regimes must
333
be modified. Due to the low nematode burden, it was not easy to evaluate which
334
of the three anthelmintic regimes was the most appropriate. Further longer
335
studies combining these and other TST criteria should be done in order to
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establish realistic parasite control strategies in areas where worm burden is
337
very low.
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ACKNOWLEDGEMENTS
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We are grateful to the INIA for funding this study (project RTA2010-00094-C03).
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We thanks to Mar Puerta, Luis Colmenar and Paloma Díez, veterinarians that
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advised us during the project and also to farmers and all the personal of the “La
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Chimenea” and IMIDRA, specially to Juan José Urquía, Ignacio Tejerina, José
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Luis Lázaro and Manuel Carpintero, that help us a lot during samplings.
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AEMET (Agencia Estatal de Meteorologia). 2011. Atlas Climatico Iberico. Ed.
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AEMET, Catalogo general de Publicaciones del Ministerio de Medio
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Bath, G.F., van Wyk, J.A., 2009. The Five Point Check© for targeted selective
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Bentounsi, B., Meradi, S., Cabaret, J., 2012. Towards finding effective
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indicators (diarrhoea and anaemia scores and weight gains) for the
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Berrag, B., Ouzir, M., Cabaret, J., 2009. A survey on meat sheep farms in two
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Gallidis, E., Papadopoulos, E., Ptochos, S., Arsenos, G., 2009. The use of
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García Romero, C., Valcárcel, F., Cordero del Campillo, M., Rojo Vázquez,
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Jackson, F., 1974. New technique for obtaining nematode ova from sheep faeces. Lab. Pract. 23, 65–66 Jackson, F., Bartley, D., Bartley, Y., Kenyon, F., 2009. Worm control in sheep in the future. Small Ruminant Res. 86, 40-45.
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Kenyon, F., Greer, A.W., Coles, G.C., Cringoli, G., Papadopoulos, E., Cabaret,
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D.J., Bartley, Y., Devin, L., Nath, M., Jackson, F., 2013. A comparative
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study of the effects of four treatment regimes on ivermectin efficacy, body weight and pasture contamination in lambs naturally infected with
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Resist. 3, 77-84. doi: 10.1016/j.ijpddr.2013.02.001.
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Martínez-Valladares, M., Valcárcel, F., Álvarez-Sánchez, M.A., Cordero-Pérez,
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P., Van Leeuwenc, J., Raji´c, A., 2012. A systematic review-meta-
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analysis of primary research investigating the effect of selected
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alternative treatments on gastrointestinal nematodes in sheep under field
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Rinaldi, L., Cringoli, G., 2012. Parasitological and pathophysiological methods
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Stafford, K.A., Morgan, E.R., Coles, G.C., 2009. Weight-based targeted
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Summers, B.A., 2009. Climate change and animal disease. Vet. Pathol. 46(6), 1185-1186. doi: 10.1354/vp.09-VP-0139-S-COM.
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Valcárcel, F., García Romero, C., 1999. Prevalence and seasonal pattern of
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anthelmintics strategies in the control of ovine trichostrongyles. Research
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Sopeña, L., Fernández Pato, N., 2013a. Atlas of Ovine Parasitology. pp.
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Martínez Valladares, M., Rojo-Vázquez, F.A., 2013b. Small ruminants
466
farm management practices in Spain and its influence on the
467
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468
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van Wyk, J.A., Hoste, H., Kaplan, R.M., Besier, R.B., 2006. Targeted selective
470
treatment for worm management-how do we sell rational programs to
471 472
Ac
469
farmers?. Vet, Parasitol. 139(4), 336-46. Epub 2006 Jun 13.
Woodgate RG, Love S. 2012. WormKill to WormBoss--can we sell sustainable
473
sheep
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474
10.1016/j.vetpar.2011.11.045.
Parasitol.
186(1-2),
51-57.
doi:
475 476 477 20 Page 21 of 35
478
TABLES
479
Table 1. Characteristics of the study flocks. Flock 1: Ovine Extensive System
481
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
482
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
483
Flock 4: Ovine Semi-extensive System
484
Flock 5CaOrSeS: Caprine Organic Semi-extensive System
485
Asl: above sea level
486
* During the previous five years egg output was regularly low or null
487
** Heaviest animals receive a higher dose
us
cr
ip t
480
an
488
Table 2. Number of animals treated using Targeted Selective Treatment
490
based on fecal egg counts, live weight loss and clinical signs; and
491
reduction
492
administered compared to a systematic treatment regime.
493
Flock 1: Ovine Extensive System
494
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
495
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
496
Flock 4: Ovine Semi-extensive System
497
Flock 5: Caprine Organic Semi-extensive System
498
EOG animals were only individually treated when elimination was equal to or higher
500 501 502 503 504 505
the
number
of
anthelmintic
treatments
ce pt
ed
in
Ac
499
(%)
M
489
than 300 GIN eggs per gram of feces (epg)
LWG animals were only individually treated when bodyweight was lower than 90% average group weight CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia) * When an animal met deworming criteria for two consecutive months, the anthelmintic treatment was only administered the first time
21 Page 22 of 35
506
In brackets is the number of animals expected to be treated using the systematic
507
treatment regime of 1.6 treatments per animal per year (Valcárcel et al., 2013b).
508 509 FIGURES
511
Figure 1. Monthly mean of Live weight, GIN, FEC and cumulative FEC for
512
20 (flock 1) and 24 months (flocks 2 and 3) of Targeted Selective
513
Treatment based on fecal egg counts, live weight loss and clinical
514
signs in three small ruminant flocks located in a low challenge
515
environment.
516
Flock 1: Ovine Extensive System
517
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
518
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
519
EOG animals were only individually treated when elimination was equal to or higher
522 523 524 525 526 527 528
cr
us
an
M
ed
LWG animals were only individually treated when bodyweight was lower than 90% of
ce pt
521
than 300 GIN eggs per gram of feces (epg)
average group weight
CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia)
* When an animal met deworming criteria for two consecutive months, the anthelmintic
Ac
520
ip t
510
treatment was only administered the first time
Numbers of legend indicate the flock number
529
Figure 2. Monthly mean of Live weight, GIN FEC and cumulative FEC for
530
12 months (flocks 4 and 5) of Targeted Selective Treatment based
531
on fecal egg counts, live weight loss and clinical signs in three
532
small ruminant flocks located in a low challenge environment. 22 Page 23 of 35
533
Flock 4: Ovine Semi-extensive System
534
Flock 5: Caprine Organic Semi-extensive System
535
EOG animals were only individually treated when elimination was equal to or higher
540 541 542 543
ip t
539
average group weight
CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia)
cr
538
LWG animals were only individually treated when bodyweight was lower than 90% of
* When an animal met deworming criteria for two consecutive months, the anthelmintic
us
537
than 300 GIN eggs per gram of feces (epg)
treatment was only administered the first time Numbers of legend indicate the flock number
an
536
544
Figure 3. Mean GIN FEC during the application of several TST protocols
546
based on fecal egg counts, live weight loss and clinical signs on
547
several small ruminant farm types. Bars with different letters are
548
significantly different.
549
Flock 1: Ovine Extensive System
550
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
551
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
552
Flock 4: Ovine Semi-extensive System
553
Flock 5: Caprine Organic Semi-extensive System
555 556 557 558 559
ed
ce pt
Ac
554
M
545
EOG animals were only individually treated when elimination was equal to or higher than 300 GIN eggs per gram of feces (epg)
LWG animals were only individually treated when body weight was lower than 90% of average group weight CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia)
23 Page 24 of 35
560 561 562
* When an animal met deworming criteria for two consecutive months, the anthelmintic treatment was only administered the first time Numbers of x asis indicate the flock number
563
ip t
564 Figure 4. Cumulative GIN FEC during the application of several TST
566
protocols based on fecal egg counts, live weight loss and clinical
567
signs on several small ruminant farm types. Bars with different letters
568
are significantly different.
569
Flock 1: Ovine Extensive System
570
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
571
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
572
Flock 4: Ovine Semi-extensive System
573
Flock 5CaOrSeS: Caprine Organic Semi-extensive System
574
EOG animals were only individually treated when elimination was equal to or higher
577 578 579 580 581 582
us an
M
ed
LWG animals were only individually treated when bodyweight was lower than 90% of
ce pt
576
than 300 GIN eggs per gram of feces (epg)
average group weight
CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia)
* When an animal met deworming criteria for two consecutive months, the anthelmintic
Ac
575
cr
565
treatment was only administered the first time
Numbers of x asis indicate the flock number
583 584 585
Figure 5. Average FEC of flocks (1 to 5) and treatment regimes (EOG, LWC, CSG).
24 Page 25 of 35
Vertical bars indicate confidence intervals at 95%. Factorial ANOVA did not find
587
differences among treatment regimes (F(2,199)=0.92; p>0.05) but it found them among
588
flocks (F(4,199)=114.21; p<0.05). Post-hoc analysis stablished three groups: A) flock 1
589
and 2; B) flock 3; C) flock 4 and 5. Threre was not interaction between factors
590
(F(8,119)=1.4; p>0.05).
591
Flock 1: Ovine Extensive System
592
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
593
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
594
Flock 4: Ovine Semi-extensive System
595
Flock 5: Caprine Organic Semi-extensive System
596
EOG animals were only individually treated when elimination was equal to or higher
average group weight
CSG animals were only individually treated when clinical signs appeared (diarrhea,
601
severe bodyweight loss or anemia)
ed
602
* When an animal met deworming criteria for two consecutive months, the anthelmintic
603
606 607 608
ce pt
605
treatment was only administered the first time
Ac
604
cr
LWG animals were only individually treated when bodyweight was lower than 90% of
599 600
us
than 300 GIN eggs per gram of feces (epg)
M
598
an
597
ip t
586
Figure 6. Saving of treatments among treatments regimes (EOG, LWG,
609
CSG).
610
Points indicate median values, rectangles indicate 25-75% of the observations and
611
vertical bars indicate minimum and maximum values. Kruskal-Wallis test found
612
significant differences among treatment regimes (H2=10.44; p<0.05) and multiple
25 Page 26 of 35
613
comparisons test founded two groups: A) corresponding to EOG, and B) corresponding
614
to CSG. LWG is between these two groups.
615
EOG animals were only individually treated when elimination was equal to or higher
619 620 621 622
average group weight
ip t
618
LWG animals were only individually treated when bodyweight was lower than 90% of
CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia)
cr
617
than 300 GIN eggs per gram of feces (epg)
* When an animal met deworming criteria for two consecutive months, the anthelmintic
us
616
treatment was only administered the first time
an
623
Ac
ce pt
ed
M
624
26 Page 27 of 35
Flock size
Flock 2 Flock 3 Government owned farm to provide selected individuals for private farmers
Ovine crossed Merino
Ovine Rubia del Molar
900
180
Flock 4 Private meat farm
Flock 5 Private organic milk farm
Ovine Colmenareña
Ovine Alcarreña
Caprine Murciano Granadina
140
2420
500
cr
Species Breed
Flock 1 Private meat farm
us
Type
ip t
Table
Extensive
Semi-extensive Semi-irrigated
Semi-extensive
Semi-extensive
Grazing
most of the time
5-6 six hours a day
5-6 hours a day
6-10 hours a day
Large open areas Continental mountain forest Sometimes shared by cattle and wild red deer
Small area Valley near the Tajo/Jarama rivers. Pasture irrigation commenced at the same time as this study. Both breeds graze together Madrid province 495m asl
mid-mountain area Small area Pastures are not shared
Pastures are not shared
Cuenca province 690m asl
Madrid province 509 m asl
Own
Outside
Reposition: Own
No*
Mid-spring and Mid-autumn
No (organic farm)
Individual weight
Average weight of flock**
-
Outside
Deworming
Mid-spring and Mid-autumn
ep te
Reposition:
M
Cuenca province 1,239m asl
d
Location:
an
System
Average weight of flock**
Check egg output before treatment?
No
Yes
Yes
No
Yes
Yes
Yes
Yes
-
12 months
12 months
3 months
3 months
Deworming reposition Age at beginning
Ac c
Dose calculation
3 months
Page 28 of 35
ip t
Table
Group size
Months of sampling
1
EOG
17
20
LWG
17
20
CSG
17
20
EOG
11
24
LWG
12
24
CSG
12
EOG
10
LWG
63.24
6 (27.2)
77.94
7 (40.8)
82.84
0 (27.2)
100.00
0 (40.8)
100.00
1 (17.6)
94.32
1 (35.2)
97.16
21.88
15 (38.4)
60.94
M
15 (19.2 0 (19.2)
100.00
0 (38.4)
100.00
24
4 (16.0)
75.00
8 (32.0)
75.00
12.50
15 (32.0)
53.13
0 (28.8)
100.00
24
0 (14.4)
100.00
18
12
0 (28.8)
100.00
20
12
17 (32.0)
46.88
CSG
19
12
0 (30.4
100.00
EOG
19
12
0 (30.4)
100.00
LWG
18
12
20 (28.8)
30.56
CSG
15
12
0 (24.0)
100.00
Ac c
5
15 (40.8)
9
LWG
% reduction
48.53
24
EOG
Number of animals treated
14 (27.2)
10
CSG 4
d
3
% reduction
During all the study
24
ep te
2
Number of animals treated
us
Deworming criterion
an
Flock
cr
During the first 12 months
14 (16.0
Page 29 of 35
50 40 30
20 10 0
F
M
A
M
J
J
A
S
O
N
D
J
F
M
A
M
J
J
A
S
500
S
O
N D
J
F M A M
J
J
A
S
O N D
J
F M A M
J
ed
150
200
100
100
50
0
F
M
A
M
J
J
A
2500
O
N
D
J
F
M
A
M
J
J
A
S
Ac
2000
S
1500 1000 500
0
J
A
S
O N
D
J
F
M A M
J
J
A
S
O N
D
J
F
M A M
J
1800
3500
1500
3000
M
A
M
J
1 EOG
J
A
S
O
N
D
J
1 LWG
M
A
M
J
J
A
1 CSG
S
A
O N D
S
J
O N D
F M A M
J
J
F M A M
J
J
A
J
S
O
N D
J
F M A M
J
A
S
O N D
J
F M A M
J
A
S
O N
J
F M A M
J
1500
600
F
J
S
2000
900
1000
300 F
A
2500
1200
0
J
700 600 500 400 300 200 100 0
200
ce pt
II. FEC (epg)
A
250
300
III. Cumulative FEC (epg)
J
300
400
0
80 70 60 50 40 30 20 10 0
us
80 70 60 50 40 30 20 10 0
60
M an
I. Live weight (kg)
70
cr
i
Figure
500 J
A
S
O
N
D
2 EOG
J
F
M A M
J
J
A
S
2 LWG
O
N
D
J
F
M A M
2 CSG
J
0
J
A
S
O N
D
3 EOG
J
F M A M
J
J
3 LWG
D
3 CSG
Page 30 of 35
Figure 1.
40
40 30
30 20
20
10
10
0
0
S
O
N
D
J
F
M
A
M
J
J
8
A
ed
4
2 0 S
O
N
D
J
F
M
A
M
J
J
20 15 10
A
M
J
J
A
S
O
N
D
J
F
140 120 100 80 60 40 20 0
A
A
M
J
J
A
S
O
N
D
J
F
120
Ac
25
ce pt
II. FEC (epg)
6
III. Cumulative FEC (epg)
cr
50
us
50
M an
I. Live weight (kg)
i
Figure
100 80 60 40
5
20
0 S
O
N
D
4 EOG
J
F
M
4 LWG
A
M
J
J
4 CSG
A
0 A
M
J
5 EOG
J
A
S
O
5 LWG
N
D
J
F
5 CSG
Page 31 of 35
Figure 2.
III: Mean FEC (epg) From 1st to 20th months (flock 1) From 1st to 24th months (flocks 2,3)
80
100
80
Figure 3. 1 EOG
ab
60
1 EOG
ab
60
40
1 EOG
60
40
20
1 LWG
20
0 1 LWG
1 LWG
1 CSG
1 CSG
1 CSG
i
b
cr
us
a
0 2 EOG
a
40
2 EOG
2 EOG
2 LWG
100
b
M an
a
ed
80
b
ce pt
I: Mean FEC (epg) from 1st to 12th month (all flocks)
100
Ac
II: Mean FEC (epg) From 13th to 20th months (flock 1) from 13th to 24th months (flocks 2, 3)
Figure
2 CSG
3 EOG
3 LWG
3 CSG
a
20
0 2 LWG
2 CSG 3 EOG 3 LWG 3 csg
2 LWG 2 CSG 3 EOG 3 LWG 3 CSG
4 EOG 4 LWG 4 CSG 5 EOG 5 LWG 5CSG
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III: Cumulative FEC (epg) From 1st to 20th months (flock 1) From 1st to 24th months (flocks 2,3)
1500
Figure 4. 2000
ab
1000
1 EOG
b
600
400
400
200
0
1 LWG
1200
1000
800
600 1 EOG 1 LWG 1 CSG
1 EOG 1 LWG 1 CSG
1 CSG
i
a
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0 2 EOG
2 EOG
2 EOG
2 LWG 2 CSG
M an
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I: Cumulative FEC (epg) From 1st to 12th months (all flocks)
1000
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II: Cumulative FEC (epg) from 13th to 20th months (flock 1) from 13th to 24th months (flocks 2, 3)
Figure
3 EOG
3 LWG
3 CSG
a
b
500
0 2 LWG
2 CSG 3 EOG 3 LWG 3 CSG
2 LWG 2 CSG 3 EOG 3 LWG 3 CSG
4 EOG 4 LWG 4 CSG 5 EOG 5 LWG 5 CSG
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Figure 5.
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Figure 6.
S0304-4017(15)00204-6 http://dx.doi.org/doi:10.1016/j.vetpar.2015.04.014 VETPAR 7606
To appear in:
Veterinary Parasitology
Received date: Revised date: Accepted date:
14-7-2014 10-4-2015 20-4-2015
Please cite this article as: Valc´arcel, F., Aguilar, A.,FIELD EVALUATION OF TARGETED SELECTIVE TREATMENTS TO CONTROL SUBCLINICAL GASTROINTESTINAL NEMATODE INFECTIONS ON SMALL RUMINANT FARMS, Veterinary Parasitology (2015), http://dx.doi.org/10.1016/j.vetpar.2015.04.014 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
*Highlights (for review)
FIELD EVALUATION OF TARGETED SELECTIVE TREATMENTS TO CONTROL SUBCLINICAL GASTROINTESTINAL NEMATODE INFECTIONS IN SMALL RUMINANT FARMS Hightlights
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We model three TST programs under five management types of small ruminants Performance and healthy status are good after TST application Regular anthelmintic dosage could not be necessary in subclinical nematodosis TST are more useful when a minimum of nematode burden is present in the farms
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*Revised Manuscript with NO changes marked (clean)
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TITLE
2
FIELD EVALUATION OF TARGETED SELECTIVE TREATMENTS TO
3
CONTROL SUBCLINICAL GASTROINTESTINAL NEMATODE INFECTIONS
4
ON SMALL RUMINANT FARMS.
AUTHORS
7
Valcárcel, F.; Aguilar, A.; Sánchez, M.
8
POSTAL ADDRESSES
9
Félix Valcárcel, [email protected]
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Ana Aguilar, [email protected]
11
María Sánchez, [email protected]
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Grupo de Parasitología Animal, Centro de Investigación en Sanidad Animal
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(INIA-CISA), 28130 Valdeolmos (Madrid), Spain.
14
CORRESPONDENCE ADDRESS
15
Félix Valcárcel Sancho DVM, PhD
16
Parasitology Group, Animal Health Research Center (INIA-CISA) 28130
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Valdeolmos (Madrid), Spain
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Tel.: 0034 91 620 23 00
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Fax: 0034 91 620 22 47
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E-mail address: [email protected]
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ABSTRACT
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Targeted selective treatments (TST) are designed to identify those
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animals that would actually benefit from anthelmintic treatment, thus reducing
24
the amount of drugs used and bringing down economic cost. In this study we
1 Page 2 of 35
assayed three TST programs based on GIN egg output, clinical sign and live
26
weight criteria in a single area where only sub-clinical infections tend to occur
27
and no Anthelmintic Resistance is reported. The study was carried out from
28
February 2011 to August 2013 on four farms applying different management
29
systems: an Ovine Extensive System, Ovine Semi-extensive Semi-irrigated
30
System focusing on “Rubia del Molar” and Colmenareña” breeds, Ovine Semi-
31
extensive System and Caprine Organic Semi-extensive System.
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The number of sheep and goats treated in all the TST strategies was
33
lower in comparison with systematic treatments, especially when selected
34
based on clinical signs (100%, in both years), followed by egg output (87.57%
35
and 90.44% in the first and second year respectively) and finally by live weight
36
(37.95% and 96.69%, in the first and second year respectively). FEC was low
37
throughout the study for all animals and groups. Apparently, the TST applied did
38
not influence live body weight.
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Preliminary results show that all three targeted selective treatments
40
significantly reduced the number of animals treated and the cost of anthelmintic
41
treatment on the farms, maintaining productivity in a low challenge environment.
42
These results also seem to indicate that systematic anthelmintic treatments are
43
unnecessary under these circumstances and traditional anthelmintic regimes
44
should therefore be modified.
45
KEY WORDS
46
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Subclinical gastrointestinal nematodosis, targeted selective treatments,
47
extensive management systems, small ruminants.
48
1. INTRODUCTION
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Like many other agricultural production sectors, sheep husbandry is
50
strongly influenced by environmental changes brought about by global climate
51
change. Climate change can lead to the emergence of new diseases or
52
changes in the prevalence of existing ones (Summers, 2009; Kenyon et al.,
53
2009a). In this context, gastrointestinal nematodes (GIN) still remain a serious
54
threat to small ruminant farming worldwide (Bentounsi et al., 2012; Mederos et
55
al., 2012). Control of parasitic infections should be based on both knowledge of
56
its
57
pharmacological products. However, most livestock producers administer
58
anthelmintic treatment without any supporting diagnostic or epidemiological
59
knowledge (Kenyon and Jackson, 2012; Valcárcel et al., 2013).
appropriate
management
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While intensive or suppressive chemical treatment strategies can give
61
rise to maximum production rates, they may not be economically sustainable
62
and could lead to anthelmintic resistance (AR). Furthermore, AR is the single
63
most important factor hindering the control of nematode parasite infection on
64
small ruminant farms (Gilleard, 2006) and is global (for a review, see Jabbar et
65
al., 2006). Therefore, a reduction in drug use is desirable to fight AR where it
66
exists and to prevent unnecessary spending on small ruminant farms. The aim
67
of targeted selective treatment (TST) is to identify those animals that could truly
68
benefit from anthelmintic treatment thus reducing the use of drugs and
69
economic cost. TST programs must be designed for each specific area and
70
treatment application indicators need to be selected carefully (Greer et al.,
71
2009). The objective is to apply the best criteria to animal selection which
72
depends on the epidemiology of the parasites and the management system
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employed (Rinaldi and Cringoli, 2012); effective application depends on the
74
accurate identification of those animals in need of anthelmintic treatment
75
(Bentounsi et al., 2012). TST programs have been successfully applied in areas where clinical
77
signs are evident and/or where AR has developed (Gallidis et al., 2009; Cringoli
78
et al., 2009; Ouzir et al., 2011; Kenyon et al., 2013). However, it is not clear
79
whether they work well in areas where GIN mainly produce subclinical
80
infections as is the case on many small ruminant farms in Europe (Kenyon and
81
Jackson, 2011; Valcárcel et al., 2013b). In this study we evaluated three TST
82
programs based on GIN egg output, clinical signs or body weight loss in one
83
area where only subclinical infections occur and no AR is reported.
84
2. MATERIALS AND METHODS
85
2.1.
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Sampling area and study farms
The study was conducted from February 2011 to August 2013 in the
87
central part of the Iberian Peninsula. According to the Köppen-Geiger
88
classification (Essenwanger, 2001; AEMET, 2011), the climate in this area is
89
Mediterranean with Continental and Atlantic influences, characterized by cold
90
winters and warm summers.
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Four farms applying different management systems were selected for the
92
study (two in the province of Cuenca and two in the province of Madrid). On one
93
of the Madrid farms, two breeds were managed and were considered separately
94
(flocks 2 and 3). So, briefly, the study was performed in five flocks: Ovine
95
Extensive System; Ovine Semi-extensive Semi-irrigated System featuring the
96
“Rubia del Molar” breed; Ovine Semi-extensive Semi-irrigated System featuring
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the “Colmenareña” breed; Ovine Semi-extensive System and Caprine Organic
98
Semi-extensive System (Flocks 1 to 5, respectively). Sampling started in
99
different months depending on when the study animals were born. Details about
101
farm characteristics and management are shown in Table 1. Study groups and sampling
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Between 51 and 64 animals per farm, depending on availability, were selected
103
for the study.
104
The condition of the animals was assessed at the beginning of the study. They
105
were weighed, individually examined by a veterinary and a fecal sample was
106
taken to evaluate GIN egg output. Selected animals from each farm were
107
distributed in three balanced groups following three TST criteria in terms of
108
body weight and faecal egg counts (FEC). All TSTs criteria were performed on
109
all the farms
110
Once selected, animals were tested every month throughout the duration of the
111
study (11 to 24 months depending on the farm). This included weighing, an
112
external veterinary inspection to detect clinical signs and the taking of individual
113
fecal samples to estimate FEC determined by means of a modified salt-
114
floatation technique with a saline solution (1.18 specific gravity) sensitive to one
115
egg per gram of feces (epg) (Jackson, 1974 and modified by Kenyon et al.,
116
2013).
117
The animals put in the three groups were managed just like the general flock
118
except for the anthelmintic treatment regime: Egg Output Group (EOG), in
119
which animals were treated individually only when elimination was equal or
120
higher than 300 GIN eggs per gram of feces (epg); Clinical Sign Group (CSG),
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in which animals were individually treated only when clinical signs were
122
observed (diarrhea, severe bodyweight loss or anemia); and Live Weight Group
123
(LWG), in which animals were individually treated only when bodyweight was
124
lower than 90% of the average weight of this group.
125
All anthelmintic treatments administered throughout the study consisted of
126
albendazole (Valbazen® 28%CO, 5 mg per kg live weight). The dose was
127
determined according to body weight measured on the day of testing. Animals
128
that met the deworming criteria for two consecutive months were only given the
129
anthelmintic treatment at first detection.
130
No other anthelmintic treatments were administered during the study.
131
2.2.
132
Parasites were identified as per Valcárcel et al. (2013a).
133
2.3.
134
The following parameters were measured when comparing study groups:
135
monthly live bodyweight; monthly, annual and global FEC; monthly, annual and
136
global cumulative FEC; clinical signs; and number of times animals were
137
dewormed. Differences between groups (p=0.05 or p<0.01) were estimated by
138
t-Student test.
139
1. Differences in FEC among Flocks and anthelmintic treatment regimes
140
In order to study differences in FEC among Flocks and anthelmintic treatment
141
regimes, a factorial-ANOVA was tested, employing average FEC in the first
142
year as a dependent variable and the flock and treatment as factors. Scheffé’s
143
test was used as a post-hoc analysis.
144
established for this analysis.
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Parasite identification
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Data analysis.
A confidence interval of 99% was
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2. Saving of the different anthelmintic treatment regimes in the first year
146
A Wilcoxon matched paired test was carried out to determine whether there
147
were significant differences between the theoretical number of treatments and
148
the number of treatments performed on each flock- anthelmintic treatment
149
regime group.
150
Two Kruskal-Wallis tests were performed to compare treatment savings among
151
flocks and among anthelmintic treatment regimes. Treatment savings are
152
defined as the percent reduction in the number of treatments actually performed
153
compared to the theoretical number of treatments. These were calculated for
154
each anthelmintic treatment regime and for each flock. A multiple comparisons
155
of mean ranks test was used as a post-Hoc test. A confidence interval of 95%
156
was established for these analyses.
157
3. RESULTS
158
3.1. Anthelmintic usage
159
The number of sheep and goats treated in accordance with TST strategies was
160
reduced compared with systematic treatments, especially where treatment was
161
based on the clinical signs criterion (100%, in both years) followed by egg
162
output (87.57% and 90.44% respectively for year one and two) and finally by
163
live weight (37.95% and 96.69% respectively).
164
The number of treatments performed was lower than the theoretical number for
165
all anthelmintic treatment groups (Table 2). The Wilcoxon matched pairs test
166
identified significant differences between the number of theoretical treatments
167
and ones actually performed in each group (W=0; p<0.05). As a consequence,
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savings from fewer treatments were statistically significant. In addition, there
169
were no significant differences in the number of treatments among flocks (H4=1,
170
p>0.05), but important differences were found among treatment regimes
171
(H2=10.44; p<0.05; Figure 6). The multiple comparisons test showed that there
172
were significant differences between the EOG anthelmintic treatment regime
173
and the CSG regime. LWG was between these two.
174
3.1.1. Egg Output anthelmintic treatment.
175
Reduction in deworming frequency based on Egg Output was quite
176
variable, ranging from 48.53% to 100% in year one and from 75% to 100%
177
in year two (Table 2).
178
A total of 19 anthelmintic treatments were administered to the EOG in year
179
one, most of them in flock 1 (14 treatments), followed by flocks 3 (4
180
treatments) and 2 (1 treatment). No anthelmintic treatments were needed
181
for the EOG in flocks 4 and 5.
182
The number of treatments administered from month 13 forward declined
183
significantly in the three flocks tested for periods longer than twelve months
184
(1 to 3); only five treatments were necessary (four in flock 3 and one in flock
185
1).
186
3.1.2. Live Weight anthelmintic regime.
187
The reduction in the number of times animals were dewormed based on the live
188
weight criterion was also very variable among the different flocks, especially in
189
year one ranging from 12.50% in flock 3 to 77.94% in flock 1.
190
The reduction was similar for the three flocks checked in year two (flocks 1, 2
191
and 3; 96.32%, 100% and 93.75%, respectively). A total of 72 and 35
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treatments were needed in the first and second years respectively. These
193
treatments were distributed throughout the year in all of the flocks.
194
3.1.3. Clinical Signs determining anthelmintic treatment.
195
The clinical signs observed were cough, nasal mucus discharge, ticks
196
presence (Hyalomma lusitanicum and Rhipicephalus bursa) and lesions in
197
oral mucosa (the latter only observed in animals from flocks 2 and 3 due to
198
a brief herbage quality) either CSG, LWG or EOG. None of the animals
199
exhibited clinical signs warranting deworming.
200
Therefore, reduction in annual anthelmintic treatment based on CSG was
201
100% for all the flocks.
202
3.2. Animal performance
203
TST did not appear to influence live bodyweight which was similar in the three
204
study groups in all the flocks (Figures 1.I and 2.I).
205
We only observed slight isolated differences in live bodyweight between LWG
206
and CSG in flock 1 from February to May during the second year (p=0.05).
207
No differences in live bodyweight were found between study groups in the other
208
flocks.
209
3.3. Parasitological results
210
3.3.1. GIN pattern
211
Through the salt-floatation analysis we regularly observed Trichostrongylidae,
212
Nematodirus, Trichuris and Moniezia eggs; Dictyocaulus and protostrongilid first
213
stage larvae; and Eimeria oocysts.
214
FEC were consistently low throughout the study in all flocks and groups
215
(Figures 1.II and 2.II) with a maximum of 275 epg in flock 1. Despite this low
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level, in year one FEC in flocks 1 to 3 exhibited a bimodal pattern with a peak
217
three months after starting to graze and a second peak five-six months later.
218
FEC was much lower as from month 13.
219
FEC in flocks 4 and 5 was very low but a small increase was observed five and
220
four months respectively after starting to graze.
221
3.3.2. Application of TST
222
Factorial ANOVA showed that there were no significant global differences
223
among treatments (F(2,199)=0.92; p>0.05), but important difference were
224
observed among flocks (F(4,199)=114.21; p<0.05; (Figure 5)). Scheffé’s test
225
identified three homogenous groups, flock 1 2 being the two flocks with higher
226
average FEC values, flock 2 had an intermediate mean value and flocks 4 and
227
5 were the two flocks with the lowest average FEC.
228
In flock 1, the mean FEC was higher (95.21 epg) when the Clinical Signs
229
criterion was applied, followed by Egg Output and lastly by Live Weight. These
230
differences with EOG (81.46 epg) and LWG (78.28 epg) were very significant
231
(p<0.01) during the first year (Figure 3.I). Either from month 13 forward (Figure
232
3.II) and during the entire study (Figure 3.III), we only observed weak
233
differences between CSG and LWG (87.90 epg; 59.64 epg, p=0.05).
234
In contrast, FEC in CSG in the other flocks was lower than in EOG and LWG
235
but the differences were not significant.
236
Similarly, we only observed weak differences (p=0.05) in cumulative FEC
237
between CSG and LWG in flock 1 during the first year (1,039.85 epg, 671.04
238
epg, Figure 4.I) and during the entire study (1,467.96 epg and 994.16 epg,
239
Figure 4.III).
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Monthly FEC and cumulative FEC of the “Colmenareña” breed (flock 3) (Figure
241
1.II) were significantly higher than in “Rubia del Molar” (flock 2) (Figure 1.III)
242
(p<0.01) as from month two and most of the following months up to the end of
243
the study (Figure 1.II and 1.III).
244
The results of fecal egg count reduction test (FECRT) in other animals from
245
flocks 1 to 3 seem to indicate that there was no presence of AR development
246
(data not shown).
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247 DISCUSSION
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249
FEC was very low throughout the study, especially during the second year, and
251
was systematically lower following the administration of Live Weight and Egg
252
Output anthelmintic treatments than after the Clinical Sign regime. These
253
results suggest a much lower worm burden than that reported in the area at the
254
end of the XXth century for both domestic and wild ruminant species (García-
255
Romero et al., 1993; Valcárcel and García Romero, 1999; Valcárcel et al.,
256
2002). Despite this fact, farmers continue applying the same anthelmintic
257
strategies and today small ruminants in the area receive 1.6 anthelmintic doses
258
per year specifically to control GIN (Valcárcel et al., 2013b). This indicates that
259
farmers are slow to assimilate change as is the case in other parts of Europe
260
(Jackson et al., 2009).
261
No treatment was administered to any of the animals in the CSG group from all
262
the flocks and they maintained low FEC, animal performance and health status,
263
suggesting a very low worm burden. Similarly, despite the fact that animals from
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the LWG group required a greater number of treatments, they did not exhibit
265
any clinical signs of GIN infection or high egg output. Smaller animals frequently
266
met the criteria for several consecutive months warranting deworming. Finally,
267
the results obtained for the EOG group are somewhere in the middle between
268
the other two.
269
FEC does not always reflect the current nematode burden (van Wyk et al.,
270
2006) but Egg Output does appear to be an accurate way of identifying animals
271
affected by worms (Gallidis et al., 2009). Theoretically, this appears to be the
272
most reasonable criterion because only those animals exhibiting a pre-defined
273
egg elimination rate are treated. However, it is more expensive because
274
requires a greater degree of animal management, regular coprological
275
analyses, etc.
276
Under the study’s subclinical infection conditions, these criteria did not appear
277
to be useful in selecting animals for deworming. However, it is important to note
278
that presumably only a small number of animals actually needed anthelmintic
279
treatment. The results from flock 1, the only one that reached a minimum
280
elimination rate during the study, seem to support this idea and better results
281
would be expected in areas with a higher nematode burden as previously
282
reported (Greer et al., 2009; Bentounsi et al., 2012; Kenyon et al., 2009b,
283
2013). Other authors reported that the Live Weight criterion is very useful in
284
identifying animals in need of treatment in areas where the worm burden is
285
large enough to produce either severe production loss or disease (Greer et al.,
286
2009, 2010; Stafford et al., 2009, Bentounsi et al., 2012) because there is
287
evidence to support the hypothesis that both of them are produced by GIN.
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TST based on a health indicator (daily weight gains) and an infection indicator
289
(number of eggs per gram of feces) can, in one grazing season, successfully
290
control anthelmintic resistance and the negative effects of nematode infections
291
(Gaba et al., 2010) and is more readily accepted by farmers needing help in
292
organizing TST (Berrag et al., 2009). The success of these approaches will
293
depend on the extra profit realized by producers (Kahn and Woodgate, 2012).
294
The benefits of a TST program only will be seen where there is a minimum
295
worm burden on the farm. It may be difficult to get farmers to accept a TST
296
program in areas where only sub-clinical infections tend to occur and/or AR
297
goes unreported. TST programs require more management procedures and the
298
reduction in the cost of anthelmintic treatments must financially offset the
299
economic cost of coprological analysis and management. Therefore, we need to
300
change the way we deliver worm control messages, properly expressing the
301
reasons to change, invisible pain, innovators and other factors (Woodgate and
302
Love, 2012).
303
With a view to improving the TST approach and making it more applicable
304
under practical farming conditions, the advantages of automated weighing
305
systems could be considered (van Wyk et al., 2006; Busin et al., 2014). A few
306
extra animals are likely to be treated unnecessarily but this will do no great
307
harm to the TST principle (Bath and van Wyk, 2009). In areas where GIN
308
infections are sub-clinical, a combination of criteria that are easy to apply and
309
acceptable by farmers would probably be most useful in targeting animals for
310
deworming; e.g. selecting only those that fulfilled the three criteria for
311
deworming and testing only during the spring and autumn seasons.
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Due the low level of elimination of Nematodirus eggs along the study it was not
313
possible to extract a conclusion about this genus. However, other parasites as
314
ticks or Protostrongylid nematodes could be important targets of parasite control
315
strategies in the area. We aware that salt-floatation technique with 1.18 specific
316
gravity is not a suitable technique to detect Protostrongylids; but the
317
appearance of L1 stages by this technique as well abundant nasal mucous
318
discharge during cold months could indicate that we should pay attention on
319
them. We also should consider the possible presence of Oestrus ovis, very
320
often in the area (Martínez-Valladares et al., 2013), as cause of this nasal
321
discharge. Unfortunately we could not perform necropsies to confirm that. In the
322
same way, we cannot be sure about the presence or absence of AR because,
323
when FECRT was performed, egg elimination were below the recommended
324
threshold for FECRT to be reliable (Coles et al., 2006).
325
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CONCLUSION
327
The preliminary results of this study in a low challenge environment show that
328
all three of the selection criteria significantly reduced the number of animals
329
treated and the cost of anthelmintic treatment maintaining productivity without
330
any disturbance of health status or production capacity. Furthermore, these
331
results also appear to indicate that systematic anthelmintic treatments are not
332
necessary under these circumstances and traditional anthelmintic regimes must
333
be modified. Due to the low nematode burden, it was not easy to evaluate which
334
of the three anthelmintic regimes was the most appropriate. Further longer
335
studies combining these and other TST criteria should be done in order to
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336
establish realistic parasite control strategies in areas where worm burden is
337
very low.
338
ACKNOWLEDGEMENTS
340
We are grateful to the INIA for funding this study (project RTA2010-00094-C03).
341
We thanks to Mar Puerta, Luis Colmenar and Paloma Díez, veterinarians that
342
advised us during the project and also to farmers and all the personal of the “La
343
Chimenea” and IMIDRA, specially to Juan José Urquía, Ignacio Tejerina, José
344
Luis Lázaro and Manuel Carpintero, that help us a lot during samplings.
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345 REFERENCES
347
AEMET (Agencia Estatal de Meteorologia). 2011. Atlas Climatico Iberico. Ed.
348
AEMET, Catalogo general de Publicaciones del Ministerio de Medio
349
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Gallidis, E., Papadopoulos, E., Ptochos, S., Arsenos, G., 2009. The use of
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Jackson, F., 1974. New technique for obtaining nematode ova from sheep faeces. Lab. Pract. 23, 65–66 Jackson, F., Bartley, D., Bartley, Y., Kenyon, F., 2009. Worm control in sheep in the future. Small Ruminant Res. 86, 40-45.
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D.J., Bartley, Y., Devin, L., Nath, M., Jackson, F., 2013. A comparative
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P., Van Leeuwenc, J., Raji´c, A., 2012. A systematic review-meta-
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alternative treatments on gastrointestinal nematodes in sheep under field
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Parasitol. 180, 372- 377.
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Rinaldi, L., Cringoli, G., 2012. Parasitological and pathophysiological methods
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Summers, B.A., 2009. Climate change and animal disease. Vet. Pathol. 46(6), 1185-1186. doi: 10.1354/vp.09-VP-0139-S-COM.
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anthelmintics strategies in the control of ovine trichostrongyles. Research
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Sopeña, L., Fernández Pato, N., 2013a. Atlas of Ovine Parasitology. pp.
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Martínez Valladares, M., Rojo-Vázquez, F.A., 2013b. Small ruminants
466
farm management practices in Spain and its influence on the
467
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468
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464
van Wyk, J.A., Hoste, H., Kaplan, R.M., Besier, R.B., 2006. Targeted selective
470
treatment for worm management-how do we sell rational programs to
471 472
Ac
469
farmers?. Vet, Parasitol. 139(4), 336-46. Epub 2006 Jun 13.
Woodgate RG, Love S. 2012. WormKill to WormBoss--can we sell sustainable
473
sheep
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Vet
474
10.1016/j.vetpar.2011.11.045.
Parasitol.
186(1-2),
51-57.
doi:
475 476 477 20 Page 21 of 35
478
TABLES
479
Table 1. Characteristics of the study flocks. Flock 1: Ovine Extensive System
481
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
482
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
483
Flock 4: Ovine Semi-extensive System
484
Flock 5CaOrSeS: Caprine Organic Semi-extensive System
485
Asl: above sea level
486
* During the previous five years egg output was regularly low or null
487
** Heaviest animals receive a higher dose
us
cr
ip t
480
an
488
Table 2. Number of animals treated using Targeted Selective Treatment
490
based on fecal egg counts, live weight loss and clinical signs; and
491
reduction
492
administered compared to a systematic treatment regime.
493
Flock 1: Ovine Extensive System
494
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
495
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
496
Flock 4: Ovine Semi-extensive System
497
Flock 5: Caprine Organic Semi-extensive System
498
EOG animals were only individually treated when elimination was equal to or higher
500 501 502 503 504 505
the
number
of
anthelmintic
treatments
ce pt
ed
in
Ac
499
(%)
M
489
than 300 GIN eggs per gram of feces (epg)
LWG animals were only individually treated when bodyweight was lower than 90% average group weight CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia) * When an animal met deworming criteria for two consecutive months, the anthelmintic treatment was only administered the first time
21 Page 22 of 35
506
In brackets is the number of animals expected to be treated using the systematic
507
treatment regime of 1.6 treatments per animal per year (Valcárcel et al., 2013b).
508 509 FIGURES
511
Figure 1. Monthly mean of Live weight, GIN, FEC and cumulative FEC for
512
20 (flock 1) and 24 months (flocks 2 and 3) of Targeted Selective
513
Treatment based on fecal egg counts, live weight loss and clinical
514
signs in three small ruminant flocks located in a low challenge
515
environment.
516
Flock 1: Ovine Extensive System
517
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
518
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
519
EOG animals were only individually treated when elimination was equal to or higher
522 523 524 525 526 527 528
cr
us
an
M
ed
LWG animals were only individually treated when bodyweight was lower than 90% of
ce pt
521
than 300 GIN eggs per gram of feces (epg)
average group weight
CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia)
* When an animal met deworming criteria for two consecutive months, the anthelmintic
Ac
520
ip t
510
treatment was only administered the first time
Numbers of legend indicate the flock number
529
Figure 2. Monthly mean of Live weight, GIN FEC and cumulative FEC for
530
12 months (flocks 4 and 5) of Targeted Selective Treatment based
531
on fecal egg counts, live weight loss and clinical signs in three
532
small ruminant flocks located in a low challenge environment. 22 Page 23 of 35
533
Flock 4: Ovine Semi-extensive System
534
Flock 5: Caprine Organic Semi-extensive System
535
EOG animals were only individually treated when elimination was equal to or higher
540 541 542 543
ip t
539
average group weight
CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia)
cr
538
LWG animals were only individually treated when bodyweight was lower than 90% of
* When an animal met deworming criteria for two consecutive months, the anthelmintic
us
537
than 300 GIN eggs per gram of feces (epg)
treatment was only administered the first time Numbers of legend indicate the flock number
an
536
544
Figure 3. Mean GIN FEC during the application of several TST protocols
546
based on fecal egg counts, live weight loss and clinical signs on
547
several small ruminant farm types. Bars with different letters are
548
significantly different.
549
Flock 1: Ovine Extensive System
550
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
551
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
552
Flock 4: Ovine Semi-extensive System
553
Flock 5: Caprine Organic Semi-extensive System
555 556 557 558 559
ed
ce pt
Ac
554
M
545
EOG animals were only individually treated when elimination was equal to or higher than 300 GIN eggs per gram of feces (epg)
LWG animals were only individually treated when body weight was lower than 90% of average group weight CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia)
23 Page 24 of 35
560 561 562
* When an animal met deworming criteria for two consecutive months, the anthelmintic treatment was only administered the first time Numbers of x asis indicate the flock number
563
ip t
564 Figure 4. Cumulative GIN FEC during the application of several TST
566
protocols based on fecal egg counts, live weight loss and clinical
567
signs on several small ruminant farm types. Bars with different letters
568
are significantly different.
569
Flock 1: Ovine Extensive System
570
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
571
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
572
Flock 4: Ovine Semi-extensive System
573
Flock 5CaOrSeS: Caprine Organic Semi-extensive System
574
EOG animals were only individually treated when elimination was equal to or higher
577 578 579 580 581 582
us an
M
ed
LWG animals were only individually treated when bodyweight was lower than 90% of
ce pt
576
than 300 GIN eggs per gram of feces (epg)
average group weight
CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia)
* When an animal met deworming criteria for two consecutive months, the anthelmintic
Ac
575
cr
565
treatment was only administered the first time
Numbers of x asis indicate the flock number
583 584 585
Figure 5. Average FEC of flocks (1 to 5) and treatment regimes (EOG, LWC, CSG).
24 Page 25 of 35
Vertical bars indicate confidence intervals at 95%. Factorial ANOVA did not find
587
differences among treatment regimes (F(2,199)=0.92; p>0.05) but it found them among
588
flocks (F(4,199)=114.21; p<0.05). Post-hoc analysis stablished three groups: A) flock 1
589
and 2; B) flock 3; C) flock 4 and 5. Threre was not interaction between factors
590
(F(8,119)=1.4; p>0.05).
591
Flock 1: Ovine Extensive System
592
Flock 2: Ovine Semi-extensive Semi-irrigated System with the “Rubia del Molar” breed
593
Flock 3: Ovine Semi-extensive Semi-irrigated System with the “Colmenareña” breed
594
Flock 4: Ovine Semi-extensive System
595
Flock 5: Caprine Organic Semi-extensive System
596
EOG animals were only individually treated when elimination was equal to or higher
average group weight
CSG animals were only individually treated when clinical signs appeared (diarrhea,
601
severe bodyweight loss or anemia)
ed
602
* When an animal met deworming criteria for two consecutive months, the anthelmintic
603
606 607 608
ce pt
605
treatment was only administered the first time
Ac
604
cr
LWG animals were only individually treated when bodyweight was lower than 90% of
599 600
us
than 300 GIN eggs per gram of feces (epg)
M
598
an
597
ip t
586
Figure 6. Saving of treatments among treatments regimes (EOG, LWG,
609
CSG).
610
Points indicate median values, rectangles indicate 25-75% of the observations and
611
vertical bars indicate minimum and maximum values. Kruskal-Wallis test found
612
significant differences among treatment regimes (H2=10.44; p<0.05) and multiple
25 Page 26 of 35
613
comparisons test founded two groups: A) corresponding to EOG, and B) corresponding
614
to CSG. LWG is between these two groups.
615
EOG animals were only individually treated when elimination was equal to or higher
619 620 621 622
average group weight
ip t
618
LWG animals were only individually treated when bodyweight was lower than 90% of
CSG animals were only individually treated when clinical signs appeared (diarrhea, severe bodyweight loss or anemia)
cr
617
than 300 GIN eggs per gram of feces (epg)
* When an animal met deworming criteria for two consecutive months, the anthelmintic
us
616
treatment was only administered the first time
an
623
Ac
ce pt
ed
M
624
26 Page 27 of 35
Flock size
Flock 2 Flock 3 Government owned farm to provide selected individuals for private farmers
Ovine crossed Merino
Ovine Rubia del Molar
900
180
Flock 4 Private meat farm
Flock 5 Private organic milk farm
Ovine Colmenareña
Ovine Alcarreña
Caprine Murciano Granadina
140
2420
500
cr
Species Breed
Flock 1 Private meat farm
us
Type
ip t
Table
Extensive
Semi-extensive Semi-irrigated
Semi-extensive
Semi-extensive
Grazing
most of the time
5-6 six hours a day
5-6 hours a day
6-10 hours a day
Large open areas Continental mountain forest Sometimes shared by cattle and wild red deer
Small area Valley near the Tajo/Jarama rivers. Pasture irrigation commenced at the same time as this study. Both breeds graze together Madrid province 495m asl
mid-mountain area Small area Pastures are not shared
Pastures are not shared
Cuenca province 690m asl
Madrid province 509 m asl
Own
Outside
Reposition: Own
No*
Mid-spring and Mid-autumn
No (organic farm)
Individual weight
Average weight of flock**
-
Outside
Deworming
Mid-spring and Mid-autumn
ep te
Reposition:
M
Cuenca province 1,239m asl
d
Location:
an
System
Average weight of flock**
Check egg output before treatment?
No
Yes
Yes
No
Yes
Yes
Yes
Yes
-
12 months
12 months
3 months
3 months
Deworming reposition Age at beginning
Ac c
Dose calculation
3 months
Page 28 of 35
ip t
Table
Group size
Months of sampling
1
EOG
17
20
LWG
17
20
CSG
17
20
EOG
11
24
LWG
12
24
CSG
12
EOG
10
LWG
63.24
6 (27.2)
77.94
7 (40.8)
82.84
0 (27.2)
100.00
0 (40.8)
100.00
1 (17.6)
94.32
1 (35.2)
97.16
21.88
15 (38.4)
60.94
M
15 (19.2 0 (19.2)
100.00
0 (38.4)
100.00
24
4 (16.0)
75.00
8 (32.0)
75.00
12.50
15 (32.0)
53.13
0 (28.8)
100.00
24
0 (14.4)
100.00
18
12
0 (28.8)
100.00
20
12
17 (32.0)
46.88
CSG
19
12
0 (30.4
100.00
EOG
19
12
0 (30.4)
100.00
LWG
18
12
20 (28.8)
30.56
CSG
15
12
0 (24.0)
100.00
Ac c
5
15 (40.8)
9
LWG
% reduction
48.53
24
EOG
Number of animals treated
14 (27.2)
10
CSG 4
d
3
% reduction
During all the study
24
ep te
2
Number of animals treated
us
Deworming criterion
an
Flock
cr
During the first 12 months
14 (16.0
Page 29 of 35
50 40 30
20 10 0
F
M
A
M
J
J
A
S
O
N
D
J
F
M
A
M
J
J
A
S
500
S
O
N D
J
F M A M
J
J
A
S
O N D
J
F M A M
J
ed
150
200
100
100
50
0
F
M
A
M
J
J
A
2500
O
N
D
J
F
M
A
M
J
J
A
S
Ac
2000
S
1500 1000 500
0
J
A
S
O N
D
J
F
M A M
J
J
A
S
O N
D
J
F
M A M
J
1800
3500
1500
3000
M
A
M
J
1 EOG
J
A
S
O
N
D
J
1 LWG
M
A
M
J
J
A
1 CSG
S
A
O N D
S
J
O N D
F M A M
J
J
F M A M
J
J
A
J
S
O
N D
J
F M A M
J
A
S
O N D
J
F M A M
J
A
S
O N
J
F M A M
J
1500
600
F
J
S
2000
900
1000
300 F
A
2500
1200
0
J
700 600 500 400 300 200 100 0
200
ce pt
II. FEC (epg)
A
250
300
III. Cumulative FEC (epg)
J
300
400
0
80 70 60 50 40 30 20 10 0
us
80 70 60 50 40 30 20 10 0
60
M an
I. Live weight (kg)
70
cr
i
Figure
500 J
A
S
O
N
D
2 EOG
J
F
M A M
J
J
A
S
2 LWG
O
N
D
J
F
M A M
2 CSG
J
0
J
A
S
O N
D
3 EOG
J
F M A M
J
J
3 LWG
D
3 CSG
Page 30 of 35
Figure 1.
40
40 30
30 20
20
10
10
0
0
S
O
N
D
J
F
M
A
M
J
J
8
A
ed
4
2 0 S
O
N
D
J
F
M
A
M
J
J
20 15 10
A
M
J
J
A
S
O
N
D
J
F
140 120 100 80 60 40 20 0
A
A
M
J
J
A
S
O
N
D
J
F
120
Ac
25
ce pt
II. FEC (epg)
6
III. Cumulative FEC (epg)
cr
50
us
50
M an
I. Live weight (kg)
i
Figure
100 80 60 40
5
20
0 S
O
N
D
4 EOG
J
F
M
4 LWG
A
M
J
J
4 CSG
A
0 A
M
J
5 EOG
J
A
S
O
5 LWG
N
D
J
F
5 CSG
Page 31 of 35
Figure 2.
III: Mean FEC (epg) From 1st to 20th months (flock 1) From 1st to 24th months (flocks 2,3)
80
100
80
Figure 3. 1 EOG
ab
60
1 EOG
ab
60
40
1 EOG
60
40
20
1 LWG
20
0 1 LWG
1 LWG
1 CSG
1 CSG
1 CSG
i
b
cr
us
a
0 2 EOG
a
40
2 EOG
2 EOG
2 LWG
100
b
M an
a
ed
80
b
ce pt
I: Mean FEC (epg) from 1st to 12th month (all flocks)
100
Ac
II: Mean FEC (epg) From 13th to 20th months (flock 1) from 13th to 24th months (flocks 2, 3)
Figure
2 CSG
3 EOG
3 LWG
3 CSG
a
20
0 2 LWG
2 CSG 3 EOG 3 LWG 3 csg
2 LWG 2 CSG 3 EOG 3 LWG 3 CSG
4 EOG 4 LWG 4 CSG 5 EOG 5 LWG 5CSG
Page 32 of 35
III: Cumulative FEC (epg) From 1st to 20th months (flock 1) From 1st to 24th months (flocks 2,3)
1500
Figure 4. 2000
ab
1000
1 EOG
b
600
400
400
200
0
1 LWG
1200
1000
800
600 1 EOG 1 LWG 1 CSG
1 EOG 1 LWG 1 CSG
1 CSG
i
a
cr
us
200
0 2 EOG
2 EOG
2 EOG
2 LWG 2 CSG
M an
ab
ce pt
800
ed
I: Cumulative FEC (epg) From 1st to 12th months (all flocks)
1000
Ac
II: Cumulative FEC (epg) from 13th to 20th months (flock 1) from 13th to 24th months (flocks 2, 3)
Figure
3 EOG
3 LWG
3 CSG
a
b
500
0 2 LWG
2 CSG 3 EOG 3 LWG 3 CSG
2 LWG 2 CSG 3 EOG 3 LWG 3 CSG
4 EOG 4 LWG 4 CSG 5 EOG 5 LWG 5 CSG
Page 33 of 35
ed ce pt Ac
FEC (epg)
M an
us
cr
i
Figure
Page 34 of 35
Figure 5.
Ac
ce pt
ed
M an
us
cr
i
Figure
Page 35 of 35
Figure 6.