Veterinary Parasitology 209 (2015) 202–209
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FAMACHA© system assessment by previously trained sheep and goat farmers in Brazil Dhéri Maia a , Fernanda Rosalinski-Moraes b , Juan Felipe de Torres-Acosta c , Maria Christine Rizzon Cintra d , Cristina Santos Sotomaior a,∗ a Graduate Program in Animal Science, School of Agricultural Sciences and Veterinary Medicine, Pontifícia Universidade Católica do Paraná (PUCPR), São José dos Pinhais, Paraná 83010-500, Brazil b Faculdade de Medicina Veterinária, Universidade Federal de Uberlândia, Ceara St, n/n, Block2T, Office 104, Uberlândia, Minas Gerais 38405-315, Brazil c Facultad de Medicina Veterinaria y Zootécnia de la Universidad Autónoma de Yucatán, Km 15.5 carretera Mérida, Xmatkuil, Mérida, Yucatán, Mexico d School of Agricultural Sciences and Veterinary Medicine, Pontifícia Universidade Católica do Paraná (PUCPR), São José dos Pinhais, Paraná 83010-500, Brazil
a r t i c l e
i n f o
Article history: Received 12 December 2014 Received in revised form 13 February 2015 Accepted 28 February 2015 Keywords: FAMACHA© Target selective treatment Learning process Farmer’s training
a b s t r a c t The aim of this study was to evaluate the degree of adoption and the correct use of the FAMACHA© system amongst sheep and goat farmers trained in a previous hands-on course. A survey was carried out with 1375 people who received FAMACHA© training from July 2009 to May 2011 in Paraná State, Brazil. The survey was conducted from March 2012 to May 2013. Firstly, a questionnaire was applied with specific questions for farmers about their anthelmintic (AH) treatment practices before and after the FAMACHA© training. In a second step, eight of the questionnaire respondents classified as sheep or goat farmers were contacted for an in loco visit during which the application of the FAMACHA© system was evaluated in the respective farms and blood samples were collected from 20 animals to calculate sensitivity and specificity. A total of 124 farmers responded the questionnaire (9% of project participants). Farmers accounted for 48.4% of total responses. Half of these farmers (51.6%) reported losses related to parasites in their property before the training. Antiparasitic treatments, at fixed intervals, were responsible for 93.1% of deworming practices before the training project. FAMACHA© was unknown for 51.7% of the respondents, and 31% knew the chart, but did not use it. After the project, 69% had adopted the system and 83% assessed the animals at regular intervals. However, 18.9% did not evaluate all animals. During the in loco visits, problems reported included the incorrect exposure of the ocular mucosa (50% of farmers) and not using the chart (87.5%). Also, 62.5% did not keep records of the FAMACHA© assessment history of the flock. However, sensitivity was 100%, with 0% false negatives. We conclude that, amongst farmers who adopted the system, despite some methodological errors regarding its use, the objectives were met in terms of reducing the number of anthelmintic treatments and providing anemic animals with AH treatment. Trained farmers seemed to require technical guidance post-training to promote effective use of the FAMACHA© system. © 2015 Elsevier B.V. All rights reserved.
∗ Corresponding author at: Graduate Program in Animal Science, School of Agricultural Sciences and Veterinary Medicine, Pontifícia Universidade Católica do Paraná – PUCPR, Rodovia BR 376 – Km 14, São José dos Pinhais, Paraná 83010-500, Brazil. Tel.: +55 41 3299 4437; fax: +55 41 3299 4363. E-mail addresses: [email protected] (D. Maia), [email protected] (F. Rosalinski-Moraes), [email protected] (J.F. de Torres-Acosta), [email protected] (M.C.R. Cintra), [email protected] (C.S. Sotomaior). http://dx.doi.org/10.1016/j.vetpar.2015.02.033 0304-4017/© 2015 Elsevier B.V. All rights reserved.
D. Maia et al. / Veterinary Parasitology 209 (2015) 202–209
1. Introduction Gastrointestinal nematodes (GIN) are the main cause of production losses in small ruminant production systems (Molento, 2009a). Reports of parasite resistance to most current drugs are found worldwide (Papadopoulos, 2008; Torres-Acosta et al., 2012a). In Brazil, the problem of anthelmintic resistance was registered since the 90s and many new reports suggest that the situation is worsening (Soccol et al., 1996; Cunha Filho et al., 1998; ThomazSoccol et al., 2004; Rosalinski-Moraes et al., 2007; Almeida et al., 2010; Veríssimo et al., 2012). Selective anthelmintic treatment of parasitized animals has been suggested as a means to increase the population of parasites in refugia (not exposed to anthelmintic treatments) (Kenyon and Jackson, 2012; Torres-Acosta et al., 2012a). The FAMACHA© system is a tool developed to identify anemic sheep and goats by evaluating the ocular mucosa when compared to a standard chart (Van Wyk and Bath, 2002). This system helps to identify animals showing signs of anemia, and possibly needing AH treatment (Van Wyk and Bath, 2002; Kenyon and Jackson, 2012). Although farmers are aware of the existence of parasite resistance to AH drugs, they are not fully convinced of the need to use a selective treatment method in their farms (Henrioud, 2011; Kenyon and Jackson, 2012; Fitzpatrick, 2013). An important factor to decide whether to adopt a selective treatment method is to reduce the cost of AH treatments (Merkel and Gipson, 2011). However, farmers are not attracted to complex GIN control strategies. At present, the strategies adopted to control GIN will require more work and monitoring (Henrioud, 2011; Woodgate and Love, 2012). The FAMACHA© system is in line with the recommendations of the Integrated Parasite Management (IPM) (FAO, 2003) as it combines regular flock monitoring, as well as the use of more than one parasite control tool, to enhance animal welfare and reduce production losses. However, the effective use of FAMACHA© demands more than proper training and a clear knowledge on the limitations of this method (Bath et al., 2001; Van Wyk and Bath, 2002; Kaplan, 2004; Ejlertsen et al., 2006; Kenyon et al., 2009; Maia et al., 2014). It is also important to identify the main constraints for trainees once they put in practice the FAMACHA© technique in their own farm. The identification of such constraints may help to strengthen future training curricula. This study aims to determine the adoption success of the FAMACHA© system by previously trained farmers. It also aims to evaluate the correct use of the FAMACHA© system in their respective farms amongst farmers who adopted this method of selective treatment.
2. Materials and methods This study was approved by the Research Ethics Committee of Pontifícia Universidade Católica do Paraná, under the Protocol 5634/11. It was also approved by the Ethics Committee on Animal Use of the same institution, under the Protocol 670.
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2.1. Database of farmers trained on the FAMACHA© system The study used the database obtained by the project “Training project for small sheep and goat producers to use the FAMACHA© system as an aid in gastrointestinal worm control” (Public Notice 07/2008 from Fundac¸ão Araucária, University Without Frontiers program) performed from July 2009 to May 2011 in the state of Paraná, Brazil. The training program was conducted on two days and consisted of a theoretical session (8 h) and a practical session (2 h). The theoretical session consisted of a workshop addressing the GIN life cycle, parasite resistance, integrated parasite management, and the use of the FAMACHA© system for the selective AH treatment. In the practical session, participants received hands-on training on the use of FAMACHA© including the direct assessment on animals (Maia et al., 2014). During this project, participants completed an application form with personal information, contacts, and professional activity (sheep farmer; goat farmer; farmer of other species; higher degree in agricultural sciences veterinarian, agronomist and animal scientist; agricultural technician; student). 2.2. Post-training questionnaire survey In March 2012, a survey was conducted to describe the GIN control strategies amongst sheep and goats farmers that received the FAMACHA© training course. It also explored the adoption of the FAMACHA© system amongst farmers. For this survey, questionnaires were submitted through electronic mail to all the project trainees. The questionnaire was also sent to city halls and offices of the Department of Agriculture and Food Supply (SEAB), in the towns where the training was held, so that the questionnaire could be distributed to all the participants (1375 people). A total of 1066 electronic questionnaires were sent and 226 questionnaires were provided through local city halls or offices of SEAB. Questionnaires consisted of 15 questions regarding their production system, methods of GIN control as well as their knowledge on parasite resistance. 2.3. Evaluation of FAMACHA© use on farm Participants who classified themselves on the training day as sheep or goat farmers were included in a second evaluation of the use of the FAMACHA© in their own farm. All farmers, even those failing to answer the questionnaire, were contacted by telephone. Those who met the established inclusion criteria were invited to participate in the study by means of in loco visits to their farm. The inclusion criteria were: (a) participating in the whole training, (b) using the FAMACHA© system routinely in their farm, and (c) having more than 20 sheep and/or goats. During the visits, a veterinarian previously trained and experienced in the use of FAMACHA© observed how farmers used the method on their animals. Issues such as animal management (use of crush, individual restraint), the correct exposure of the lower eyelid mucosa, or whether the chart was used or
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not, were assessed. The farmer evaluated 20 animals and, at the end of the assessment, the veterinarian inspected the lower eyelid mucosa of animals correctly applying the FAMACHA© system (Van Wyk and Bath, 2002). Then, the veterinarian collected blood samples for the microhematocrit determination. Blood collection was performed by puncture of the external jugular vein using Vacutainer® tubes with anticoagulant (EDTA). The blood was used to determine the hematocrit value (Ht) as proposed by Jain (1986). At the end of the visit, farmers were interviewed again, with questions regarding satisfaction with the FAMACHA© system, frequency of use, the existence of a record of FAMACHA© scores in the flock, the use of AH and the existence of technical assistance in the farm. 2.4. Statistical analyses The questionnaires of the two stages were tabulated in spreadsheets of the software Microsoft Excel. Univariate and bivariate analysis of answers were performed. Practices adopted for deworming the flocks before and after the training were analyzed by means of respective chi-square tests, with 5% level of significance, using Statgraphics Centurion XVI. FAMACHA© grades assigned by farmers and the hematocrit results of each animal were used to determine sensitivity and specificity values and to observe whether animals were truly anemic, thus, whether the AH treatments were correctly applied. The hematocrit pattern established to confirm anemia, for the sensitivity and specificity tests, was the value ≤18%, since it is the boundary between categories 3 and 4 of the FAMACHA© system (Kaplan et al., 2004). Two criteria were established for calculations: (a) animals classified as FAMACHA© 4 and 5 regarded as anemic, and (b) animals classified as FAMACHA© 3, 4, and 5 regarded as anemic. The sensitivity and specificity values were calculated according to Vatta et al. (2001) and Thrusfield (2005). True positive (TP) were anemic animals identified as such, i.e. animals with hematocrit ≤18% and classified as FAMACHA© 4 and 5, or 3, 4, and 5. True negative (TN) were animals that show no anemia (Ht > 18), i.e. classified as FAMACHA© 1 and 2, or 1, 2, and 3. False positive (FP) values were non-anemic animals with FAMACHA© grades suggestive of anemia. False negative (FN) are anemic animals not identified by the system. When using the FAMACHA© system, sensitivity indicated the proportion of anemic animals correctly identified [SEN = TP × 100/(TP + FN)] and specificity indicated the proportion of non-anemic animals correctly identified [SPE = TN × 100/(TN + FP)]. 3. Results and discussion 3.1. Practices for parasite control From the 1375 people that participated in the training project, a total of 124 people responded the questionnaire totaling 9% of participants. Out of the 124 respondents, 60 (48.4%) were sheep and/or goat farmers, corresponding to 21.3% of farmers trained through the project. Although
farmers represented a smaller proportion of trainees in the project (20.4% of the total), they accounted for nearly half of respondents, which suggests that farmers were more interested in responding to the questionnaire than veterinarians, animal scientists, agriculturalists, agricultural technicians or students. The participation obtained in this study is similar to that found by other workers when applying their questionnaires only to farmers in the UK (McMahon et al., 2013) or the in United States (Merkel and Gipson, 2011). Specific questions were asked to participants who classified themselves as sheep and/or goat farmers. According to the responses obtained from farmers, 83.3% (n = 50) of flocks are aimed at meat production, 10.1% (n = 6) aimed at other purposes such as wool production, research and leisure, followed by 6.6% (n = 4) properties specialized in producing purebreds. Despite the fact that anthelmintic resistance associated with production losses arising from verminosis constitute a major problem for small ruminant production in Paraná and around the world (Kaplan, 2004; Thomaz-Soccol et al., 2004; Papadopoulos, 2008; Kaplan and Vidyashankar, 2012; Torres-Acosta et al., 2012a), only 51.6% of respondents reported losses in their property related to worms. This percentage may be due to non-evident production losses, which are difficult to identify, unlike what happens with death animals. It is difficult for producers to quantify the actual impact of GIN on health and productivity of their animals because these parasites are internal (Torres-Acosta et al., 2012b). Before the training project (considering a total of 58 respondent farmers) mass AH treatment of the entire flock for the control of GIN was performed at regular intervals by 93.1% of the farmers (n = 54). Table 1 shows that AH treatments were applied using the following criteria: (a) monthly treatments (34,5%), (b) when clinical signs of worms were apparent (diarrhea, submandibular edema, low body condition score) (29.3%), (c) according to the management of the flock (breeding season, before birth, at weaning) (27.6%), (c) using FAMACHA© (6.9%). None of the surveyed farmers used the FEC as a criteria for AH treatment. The latter suggests that farmers were not concerned or ignored that such mass treatments lead to the selection of worms resistant to AH drugs. This is consistent with findings in Spain by Rojo-Vázquez and Housking (2013) who reported that approximately a third of producers have no knowledge on anthelmintic resistance in their property, and this fact does not seem to be a main concern. Table 1 also shows that over half of the responding farmers (n = 30; 51.7%) did not know the FAMACHA© system before the training project and 31% (n = 18) claimed to know the system, but did not use it. Poor knowledge and adoption of the system may be related to its recent introduction to this area of Brazil. The first studies were conducted in 2003 and 2004 (Sotomaior et al., 2003; Molento et al., 2004), while the concept of deworming the entire flock to control worms was widely recommended for decades. Furthermore, adopting a new technology, that is more time consuming than mass treatment schemes, is less attractive for farmers and technicians than keeping old practices (Henrioud, 2011). Amongst 17.2% (n = 10) of farmers who claimed to know and use the FAMACHA© system before the
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Table 1 Knowledge on the FAMACHA© system for controlling worms in small ruminants and its use compared to deworming practices applied to the flock before the training course, according to a questionnaire answered by the course participants in the State of Paraná, Brazil. Deworming strategy before the course
Knew FAMACHA© before the course
No
Yes, did not use
Total
Yes, without chart
Yes, photocopy
Yes, purchase chart
Monthly When there were signs of worms According to management Using FAMACHA© According to fecal egg counts Another
11 (19.0%) 11 (19.0%)
4 (6.9%) 6 (10.3%)
4 (6.9%) 0 (0.0%)
1 (1.7%) 0 (0.0%)
0 (0.0%) 0 (0.0%)
20 (34.5%) 17 (29.3%)
6 (10.3%)
8 (13.8%)
1 (1.7%)
0 (0.0%)
1 (1.7%)
16 (27.6%)
1 (1.7%) 0 (0.0%)
0 (0.0%) 0 (0.0%)
3 (5.2%) 0 (0.0%)
0 (0.0%) 0 (0.0%)
0 (0.0%) 0 (0.0%)
4 (6.9%) 0 (0.0%)
1 (1.7%)
0 (0.0%)
0 (0.0%)
0 (0.0%)
0 (0.0%)
1 (1.7%)
Total
30 (51.7%)
18 (31.0%)
8 (13.8%)
1 (1.7%)
1 (1.7%)
58 (100%)
Obs.: all percentages were calculated regarding the total number of answers obtained (58).
training project, most of them did not use the chart during animal assessment (n = 8), and only 1 of the remaining 2 farmers used the official chart (Table 1). Failure to use the FAMACHA© chart as a standard reference of this method (Van Wyk and Bath, 2002) during animal assessments suggest that farmers were exposed to the FAMACHA© system by means failing to provide the chart. The latter is consistent with previous surveys reporting that the main information source for farmers consisted of newspapers, leaflets, pharmaceutical industry, and guidance by other people (Cabaret et al., 2009; McMahon et al., 2013). Before the training project, monthly treatments took place in 34.5% of flocks, and other deworming criteria corresponding to a frequent treatment interval, including treatments every 15 days, every 40 days and bimonthly (Table 1). In the state of Minas Gerais, Brazil, studies involving management practices amongst goat farmers showed that 83% of meat farmers answered to use frequent dewormings in their entire flock, at intervals ranging from 1 month (1–2 months = 48.8%) to more than 4 months
(2.4%) (Guimarães et al., 2011). Similar results were found in sheep flocks in the state of Rio de Janeiro, Brazil, where Cruz et al. (2010) obtained results such as 97% of farmers using dewormings as a way for controlling gastrointestinal worms, the vast majority on a monthly or bimonthly basis (38%). The frequency of AH treatments applied before the training project can be observed in Table 2. Selective treatment was performed by few farmers (20.7%) irrespective of the criteria of treatment used to decide treatment. This indicated that some farmers were already aware of the need to treat only the animals needing treatment. Table 2 also shows that most deworming criteria, concerning which animals were treated, changed after the training (p < 0.0001). Farmers were treating all the animals before the FAMACHA© course (67.2%) and this radically reduced after the course to only 12.1% of farmers. Similarly, the number of people that treated the animals selectively increased from 20.7% to 75.9%. These data suggest again that the course created awareness amongst
Table 2 Practices adopted for deworming flocks before and after the course, regarding the number of small ruminants dewormed, according to a questionnaire sent to participants in the FAMACHA© training course in the State of Paraná, Brazil. Deworming criteria
Which animals Selective
Total All the animals
Per group or category
4 (6.9%) 3 (5.2%) 3 (5.2%) 0 (0.0%) 2 (3.4%) 0 (0.0%)
0 (0.0%) 8 (13.8%) 12 (20.7%) 0 (0.0%) 18 (31.0%) 1 (1.7%)
0 (0.0%) 5 (8.6%) 2 (3.4%) 0 (0.0%) 0 (0.0%) 0 (0.0%)
4 (6.9%) 16 (27.6%) 17 (29.3%) 0 (0.0%) 20 (34.5%) 1 (1.7%)
Total
12 (20.7%)
39 (67.2%)
7 (12.1%)
58 (100%)
After the course Using FAMACHA© According to management When there are signs of worms According to fecal egg counts Monthly
33 (56.9%) 6 (10.3%) 4 (6.9%) 1 (1.7%) 0 (0.0%)
2 (3.4%) 1 (1.7%) 2 (3.4%) 0 (0.0%) 2 (3.4%)
5 (8.6%) 1 (1.7%) 0 (0.0%) 0 (0.0%) 1 (1.7%)
40 (69.0%) 8 (13.8%) 6 (10.3%) 1 (1.7%) 3 (5.2%)
Total
44 (75.9%)
7 (12.1%)
7 (12.1%)
58 (100%)
Before the course Using FAMACHA© According to management When there are signs of worms According to fecal egg counts Monthly Another
Obs.: all percentages were calculated regarding the total number of answers obtained (58).
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farmers that the selective treatment was feasible and desirable. When comparing the deworming methods adopted by farmers before and after the course, it is evident that there was a substantial change (p < 0.0001). After training, 69.0% dewormed according to FAMACHA© . The latter can be considered a great success because only 6.9% of farmers used that technique before the course (Table 2). As a direct consequence, all the other deworming criteria were significantly reduced: (a) monthly treatments was reduced from 34.5% to only in 5.2% of farmers, (b) treatment according to management reduced from 27.6% to 13.8% of farmers and (c) treatments according to signs reduced from 29.3% to 10.3% (p < 0.0001). The level of adoption found in the present study is higher than that reported in previous studies performed in Brazil. In the state of São Paulo, Brazil, 47.1% of flocks surveyed used the FAMACHA© system as a deworming criterion and the signs of worms are taken into account in 41.2% of cases (Veríssimo et al., 2012). On the other hand, Cruz et al. (2010) reported only 3% of FAMACHA© use as a criterion for deworming sheep in Rio de Janeiro. It seems that the higher adoption reported for farmers in Paraná is the result of the FAMACHA© training course. These questionnaire surveys performed in Brazil (São Paulo and Rio de Janeiro) reported the adoption of farmers that did not receive a previous training. Amongst those who did not adopt the system, the main reasons were: (a) time spent for evaluating animals is too long, (b) it is difficult to assess animals by a sole person, and (c) farmers attempt to avoid animal stress. The time constraint has been mentioned as an important reason to resist the adoption of selective anthelmintic treatment schemes, since they require more effort to monitor the flock’s health (Cabaret et al., 2009; Torres-Acosta et al., 2014). The present survey showed that farmers were able to establish a routine to use the FAMACHA© system since 83% of assessments have occurred at monthly intervals or sooner. Meanwhile, around 9.4% of farmers reported that assessments were performed less frequently (from 40 to 90 days). During the training course, the period recommended as ideal was three weeks. Van Wyk and Bath (2002) reported that, for reducing risk of clinical nematodosis in this system, the assessment must be used at short time intervals (from 7 to 14 days), especially during periods with high parasite challenge, corroborating the findings of Burke et al. (2007) and Reynecke et al. (2011). However, a long-term trial testing a targeted selective AH treatment scheme in the tropics of México showed that animal assessments could be performed once every month without evidence of negative consequences for the animals (Torres-Acosta et al., 2014). Finally, up to 7.5% of farmers still reported other criteria to perform the FAMACHA© evaluation (management change and emergency of clinical signs compatible with GIN infection). As for the assessment criterion of the entire flock or a part of it, the FAMACHA© system was applied to all animals in 81.1% of properties. Failing to use it in all the flock seemed to be unrelated to the number of animals (Table 3). At first, there should be no reason for not evaluating all animals, especially in small flocks, such as in most cases in this study. According to Bath et al. (2001), those farms with
sufficient facilities and with experienced personnel allowing, one person who is experienced in the use of the system can inspect more than 500 sheep per hour. For using the FAMACHA© system, recommendations to deworm sheep are always to deworm animals classified as 4 and 5 and in some cases, those classified as 3 (Van Wyk and Bath, 2002). On the other hand, dewormings of goats should always be applied to animals classified as 3, 4, and 5 (Vatta et al., 2001; Van Wyk and Bath, 2002; Mahieu et al., 2007; Sotomaior et al., 2012). According to Table 4, it was observed that 28.3% of dewormings involved only animals classified as 4 and 5. For goats and sheep, the inclusion of deworming in FAMACHA© 3 significantly increases the sensitivity levels of the system (Burke et al., 2007; Reynecke et al., 2011; Sotomaior et al., 2012; Torres-Acosta et al., 2014) but increased the proportion of animals that are supposed to be treated with an AH.
3.2. Use of FAMACHA© by farmers Eight farmers who took part in the theoretical and practical aspects of the FAMACHA© training project were selected for the in loco evaluation. The small number of assessments was due to the difficulty to contact producers. Some farmers were not receptive to sample collection in their property, and, finally, some of them did not have the minimum number of 20 animals. Although all the training participants received the official FAMACHA© chart, its use for evaluating animals was neglected in most cases (87.5%) (Table 5). It is possible that, due to the system’s simplicity, many farmers rely on their memory when evaluating animals. This practice can lead to errors, since colors on the chart are the basis of the FAMACHA© methodology (Bath et al., 2001; Van Wyk and Bath, 2002). During on-farm assessments, farmers fail to provide the correct exposure of animal’s ocular mucosa and they also fail to use the chart. Only 50% of farmers exposed the animal’s ocular mucosa for proper analysis, pressing carefully the upper eyelid and pulling the lower eyelid. The mistake made by the rest of farmers was evaluating with an open upper eyelid. Although farmers were shown how to correctly perform the eye lid and expose the mucosa in their animals, farmers did not practice during training the correct eye opening technique. Thus, it is clear that course participants must practice the correct way of exposing the conjunctival mucosa during the hands-on classes, as indicated by Molento (2009b). Although Kaplan et al. (2004) demonstrated the effectiveness of the use of the system by trained farmers, observed mistakes indicate the need for technical supervision on-farm during a period of “adoption”. The latter suggests that regular calibration (i.e. determination of the relationship between FAMACHA© scoring and the hematocrit gold standard) of the FAMACHA© scoring process amongst trained personnel is essential, since there is a tendency of making mistakes in the classifications (Reynecke et al., 2011). It is important to indicate that, the only case in which errors during training were lower than posttraining, took place in a property that received technical assistance on a monthly basis.
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Table 3 Use of the FAMACHA© system and assessment of the entire flock or a part of it, with regard to the number of animals in the farm, according to the questionnaire sent to participants in the FAMACHA© training course in the State of Paraná, Brazil. Assessment of all animals using FAMACHA©
Number of animals
Yes
Total
Only those that seem to be sick
Less than 20 animals 20–49 animals 50–99 animals 100–499 animals 500–999 animals
17 (32.1%) 7 (13.2%) 9 (17.0%) 9 (17.0%) 1 (1.9%)
2 (3.8%) 5 (9.4%) 1 (1.9%) 2 (3.8%) 0 (0.0%)
19 (35.8%) 12 (22.6%) 10 (18.9%) 11 (20.8%) 1 (1.9%)
Total
43 (81.1%)
10 (18.9%)
53 (100%)
Obs.: all percentages were calculated regarding the total number of answers obtained (58). Table 4 Deworming according to the various grades of FAMACHA© in sheep and goats, according to a questionnaire sent to participants in the FAMACHA© training course, in the State of Paraná, Brazil. FAMACHA© category dewormed
Species of ruminant
Total
4 and 5
4 and 5, in some cases, 3
3, 4, and 5
Sheep Goats Sheep and goats
10 (18.9%) 0 (0.0%) 5 (9.4%)
18 (34.0%) 0 (0.0%) 8 (15.1%)
8 (15.1%) 1 (1.9%) 3 (5.7%)
36 (67.9%) 1 (1.9%) 16 (30.2%)
Total
15 (28.3%)
26 (49.1%)
12 (22.6%)
53 (100%)
Obs.: all percentages were calculated regarding the total number of answers obtained (53).
The absence of a data record system for the FAMACHA© assessments, production and reproductive performance was recorded in 62.5% of properties visited (Table 5). The latter is an important problem as farmers cannot identify those animals recurrently identified with FAMACHA© 4 or 5. This represents a clear disadvantage for farmers, as they cannot eliminate these problematic animals. One advantage of the system is the genetic selection of resistant and resilient animals in the long term (Van Wyk and Bath, 2002; Riley and Van Wyk, 2009), this opportunity was neglected in these cases. Despite the problems mentioned above, the results shown in Table 6 indicated that there were no cases of animals classified as false negatives, i.e. non-anemic animal failing to be dewormed. Producers trained in the United States of America obtained 2.7% of FN assessments, considering Ht ≤ 19 and deworming animals classified as 4 and 5, and 0.6% of FN when animals classified as 3, 4, and 5 were treated (Kaplan et al., 2004). However, there were large numbers of animals receiving unnecessary treatments (FP). Irrespective of the problems mentioned above, the use of the FAMACHA© system is in line with what has been
currently sought for the control gastrointestinal worms, i.e. reducing the number of animals receiving an AH treatment. Providing anthelmintic treatment to 11.9–36.9% of the animals, even when some did not need it, is better than providing treatment to 100% of animals every month. The part of the flock that was not dewormed will contribute to keep the refugia population (Van Wyk, 2001; Van Wyk and Bath, 2002; Kenyon et al., 2009; Besier, 2012). The sensitivity of the system was 100% both, when the deworming of animals level 3 was included, and when only those animals with FAMACHA© 4 and 5 were dewormed. Specificity, however, decreased from 87.8% to 62.42% when FAMACHA© 3 animals were treated. Considering Ht ≤ 19, Kaplan et al. (2004) obtained sensitivity results of 92.2% and 64.1% including and not including the deworming of sheep classified as level 3, respectively. The latter is very similar to the sensitivities (96.9% and 60.9%) reported for goats under tropical conditions by Torres-Acosta et al. (2014), using a Ht < 22. A high sensitivity when using the FAMACHA© system is a desirable factor, because the animals that need deworming do not fail to be treated. Failure to deworm an animal regarded as false negative
Table 5 Data from the farmer’s interviews and the in loco assessment of eight sheep and goat farmers on the use of the FAMACHA© system and property characteristics of farms. Topics evaluated
Number of animals Use of the chart Opens the eye correctly Assessment frequency Recording system Crush Assistance Dewormed
Farmers interviewed and visited A
B
C
D
E
F
G
H
500–999 If in doubt Yes 15 days Yes Yes Monthly 3, 4, 5
50–99 Sometimes Yes 15–30 days Yes No No 2, 3, 4, 5
≤20 Sometimes Yes 60 days No No No 3, 4, 5
≤20 Sometimes Yes 60 days No No No 3, 4, 5
50–99 Yes No 30 days Yes No No 3, 4, 5
100–499 No No When sick No No No 3, 4, 5
20–49 Sometimes No When sick No No No 4, 5
20–49 Sometimes No When sick No No No 4, 5
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Table 6 Values of false negative (FN), false positive (FP), true positive (TP), and true negative (TN) sheep according to the hematocrit value and deworming the animals classed as FAMACHA© 3, 4, and 5 or those classified as 4 and 5 by producers previously trained and evaluated in the state of Paraná, Brazil. Ht
Dewormed
FN
FP
TP
TN
Total
≤18 ≤18
3, 4, and 5 4 and 5
0 0
59 (36.9%) 19 (11.9%)
3 (1.9%) 3 (1.9%)
98 (61.2%) 138 (86.2%)
160 160
may lead to production losses and even death (Vatta et al., 2001; Kaplan et al., 2004).
4. Conclusion People who attended the FAMACHA© training declared that after the course they started to deworm their animals using criteria that could help to maintain a higher proportion of the nematode population in the refugia (that is, untreated) than would be the case if treatment of the whole flock were practised. However, most farmers tended to simplify the FAMACHA© methodology by not using the chart or not keeping a written history of animals dewormed, and half of the farmers had an incorrect technique to expose the ocular mucosa. All these aspects compromise the long-term use of the FAMACHA© system. Errors regarding the use of FAMACHA© on-farm by the trained farmers suggested that training must be improved. Furthermore, there is a need for post-training on-farm monitoring on the correct use of the FAMACHA© system. In spite of the errors detected, farmers detected all anemic animals when evaluated on-farm (100% sensitivity).
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D. Maia et al. / Veterinary Parasitology 209 (2015) 202–209 Soccol, V.T., Sotomaior, C.S., Souza, F.P., Castro, E.A., Pessôa Silva, M.C., Milczewski, V., 1996. Occurence of resistance to anthelmintics in sheep in Paraná State, Brazil. Vet. Rec. 139, 421–422. Sotomaior, C.S., Milczewski, V., Schwartz, M.G., Moraes, F.R., 2003. Evaluation of FAMACHA System: accuracy of anaemia estimation and use of the method on commercial sheep flocks. In: Proceedings International Seminar in Animal Parasitology, 5, 2003, Merida. SENASICA-INIFAPINFARVET-UADY-FAO-AMPAVE, Merida, pp. 61–66. Sotomaior, C.S., Rosalinski-Moraes, F., Costa, A.R.B., Maia, D., Monteiro, A.L., Van Wyk, J.A., 2012. Sensitivity and specificity of the FAMACHA© system in Suffolk sheep and crossbred Boer goats. Vet. Parasitol. 190, 114–119. Thomaz-Soccol, V., Souza, F.P., Sotomaior, C.S., Castro, E.A., Milczewski, V., Mocelin, G., Silva, M.P., 2004. Resistance of gastrointestinal nematodes to anthelmintics in sheep (Ovis aries). Braz. Arch. Biol. Technol. 47, 41–47. Thrusfield, M.V., 2005. Veterinary Epidemiology. Blackwell, Cambridge, 610 pp. Torres-Acosta, J.F.J., Mendoza-de-Gives, P., Aguillar-Caballero, A.J., Cuellar-Ordaz, J.A., 2012a. Anthelmintic resistance in sheep farms: update of the situation in the American continent. Vet. Parasitol. 189, 89–96. Torres-Acosta, J.F.J., Molento, M., Mendoza-de-Gives, P., 2012b. Research and implementation of novel approaches for the control of nematode
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parasites in Latin America and the Caribbean: is there sufficient incentive for a greater extension effort? Vet. Parasitol. 186, 132–142. Torres-Acosta, J.F.J., Pérez-Cruz, M., Canul-Ku, H.L., Soto-Barrientos, N., Cámara-Sarmiento, R., Aguilar-Caballero, A.J., Lozano-Argáes, I., LeBigot, C., Hoste, H., 2014. Building a combined targeted selective treatment scheme against gastrointestinal nematodes in tropical goats. Small Rumin. Res. 121, 27–35. Van Wyk, J.A., 2001. Refugia – overlooked as perhaps the most important factor concerning the development of anthelmintic resistance. Onderstepoort J. Vet. Res. 68, 55–57. Van Wyk, J.A., Bath, G.F., 2002. The FAMACHA system for managing haemonchosis in sheep and goats by clinically identifying individual animals for treatment. Vet. Res. 33, 509–529. Vatta, A.F., Letty, B.A., Van der Linde, M.J., Van Wyk, E.F., Hansen, J.W., Krecek, R.C., 2001. Testing for clinical anaemia caused by Haemonchus spp. in goats farmed under resource-poor conditions in South Africa using an eye colour chart developed for sheep. Vet. Parasitol. 99, 1–14. Veríssimo, C.J., Niciura, S.C.M., Alberti, A.L.L., Rodrigues, C.F.C., Barbosa, D.P.C., Chartoso, D., Silva, G.S., Pereira, J.R., Margatho, L.F.F., Costa, R.L.D., Nardon, R.F., Ueno, T.E.H., Cursi, V.C.L.M., Molento, M.B., 2012. Multidrug and multispecies resistance in sheep flocks from Sao Paulo state, Brazil. Vet. Parasitol. 187, 209–216. Woodgate, R.G., Love, S., 2012. WormKill to WormBoss – can we sell sustainable sheep worm control? Vet. Parasitol. 186, 51–57.
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FAMACHA© system assessment by previously trained sheep and goat farmers in Brazil Dhéri Maia a , Fernanda Rosalinski-Moraes b , Juan Felipe de Torres-Acosta c , Maria Christine Rizzon Cintra d , Cristina Santos Sotomaior a,∗ a Graduate Program in Animal Science, School of Agricultural Sciences and Veterinary Medicine, Pontifícia Universidade Católica do Paraná (PUCPR), São José dos Pinhais, Paraná 83010-500, Brazil b Faculdade de Medicina Veterinária, Universidade Federal de Uberlândia, Ceara St, n/n, Block2T, Office 104, Uberlândia, Minas Gerais 38405-315, Brazil c Facultad de Medicina Veterinaria y Zootécnia de la Universidad Autónoma de Yucatán, Km 15.5 carretera Mérida, Xmatkuil, Mérida, Yucatán, Mexico d School of Agricultural Sciences and Veterinary Medicine, Pontifícia Universidade Católica do Paraná (PUCPR), São José dos Pinhais, Paraná 83010-500, Brazil
a r t i c l e
i n f o
Article history: Received 12 December 2014 Received in revised form 13 February 2015 Accepted 28 February 2015 Keywords: FAMACHA© Target selective treatment Learning process Farmer’s training
a b s t r a c t The aim of this study was to evaluate the degree of adoption and the correct use of the FAMACHA© system amongst sheep and goat farmers trained in a previous hands-on course. A survey was carried out with 1375 people who received FAMACHA© training from July 2009 to May 2011 in Paraná State, Brazil. The survey was conducted from March 2012 to May 2013. Firstly, a questionnaire was applied with specific questions for farmers about their anthelmintic (AH) treatment practices before and after the FAMACHA© training. In a second step, eight of the questionnaire respondents classified as sheep or goat farmers were contacted for an in loco visit during which the application of the FAMACHA© system was evaluated in the respective farms and blood samples were collected from 20 animals to calculate sensitivity and specificity. A total of 124 farmers responded the questionnaire (9% of project participants). Farmers accounted for 48.4% of total responses. Half of these farmers (51.6%) reported losses related to parasites in their property before the training. Antiparasitic treatments, at fixed intervals, were responsible for 93.1% of deworming practices before the training project. FAMACHA© was unknown for 51.7% of the respondents, and 31% knew the chart, but did not use it. After the project, 69% had adopted the system and 83% assessed the animals at regular intervals. However, 18.9% did not evaluate all animals. During the in loco visits, problems reported included the incorrect exposure of the ocular mucosa (50% of farmers) and not using the chart (87.5%). Also, 62.5% did not keep records of the FAMACHA© assessment history of the flock. However, sensitivity was 100%, with 0% false negatives. We conclude that, amongst farmers who adopted the system, despite some methodological errors regarding its use, the objectives were met in terms of reducing the number of anthelmintic treatments and providing anemic animals with AH treatment. Trained farmers seemed to require technical guidance post-training to promote effective use of the FAMACHA© system. © 2015 Elsevier B.V. All rights reserved.
∗ Corresponding author at: Graduate Program in Animal Science, School of Agricultural Sciences and Veterinary Medicine, Pontifícia Universidade Católica do Paraná – PUCPR, Rodovia BR 376 – Km 14, São José dos Pinhais, Paraná 83010-500, Brazil. Tel.: +55 41 3299 4437; fax: +55 41 3299 4363. E-mail addresses: [email protected] (D. Maia), [email protected] (F. Rosalinski-Moraes), [email protected] (J.F. de Torres-Acosta), [email protected] (M.C.R. Cintra), [email protected] (C.S. Sotomaior). http://dx.doi.org/10.1016/j.vetpar.2015.02.033 0304-4017/© 2015 Elsevier B.V. All rights reserved.
D. Maia et al. / Veterinary Parasitology 209 (2015) 202–209
1. Introduction Gastrointestinal nematodes (GIN) are the main cause of production losses in small ruminant production systems (Molento, 2009a). Reports of parasite resistance to most current drugs are found worldwide (Papadopoulos, 2008; Torres-Acosta et al., 2012a). In Brazil, the problem of anthelmintic resistance was registered since the 90s and many new reports suggest that the situation is worsening (Soccol et al., 1996; Cunha Filho et al., 1998; ThomazSoccol et al., 2004; Rosalinski-Moraes et al., 2007; Almeida et al., 2010; Veríssimo et al., 2012). Selective anthelmintic treatment of parasitized animals has been suggested as a means to increase the population of parasites in refugia (not exposed to anthelmintic treatments) (Kenyon and Jackson, 2012; Torres-Acosta et al., 2012a). The FAMACHA© system is a tool developed to identify anemic sheep and goats by evaluating the ocular mucosa when compared to a standard chart (Van Wyk and Bath, 2002). This system helps to identify animals showing signs of anemia, and possibly needing AH treatment (Van Wyk and Bath, 2002; Kenyon and Jackson, 2012). Although farmers are aware of the existence of parasite resistance to AH drugs, they are not fully convinced of the need to use a selective treatment method in their farms (Henrioud, 2011; Kenyon and Jackson, 2012; Fitzpatrick, 2013). An important factor to decide whether to adopt a selective treatment method is to reduce the cost of AH treatments (Merkel and Gipson, 2011). However, farmers are not attracted to complex GIN control strategies. At present, the strategies adopted to control GIN will require more work and monitoring (Henrioud, 2011; Woodgate and Love, 2012). The FAMACHA© system is in line with the recommendations of the Integrated Parasite Management (IPM) (FAO, 2003) as it combines regular flock monitoring, as well as the use of more than one parasite control tool, to enhance animal welfare and reduce production losses. However, the effective use of FAMACHA© demands more than proper training and a clear knowledge on the limitations of this method (Bath et al., 2001; Van Wyk and Bath, 2002; Kaplan, 2004; Ejlertsen et al., 2006; Kenyon et al., 2009; Maia et al., 2014). It is also important to identify the main constraints for trainees once they put in practice the FAMACHA© technique in their own farm. The identification of such constraints may help to strengthen future training curricula. This study aims to determine the adoption success of the FAMACHA© system by previously trained farmers. It also aims to evaluate the correct use of the FAMACHA© system in their respective farms amongst farmers who adopted this method of selective treatment.
2. Materials and methods This study was approved by the Research Ethics Committee of Pontifícia Universidade Católica do Paraná, under the Protocol 5634/11. It was also approved by the Ethics Committee on Animal Use of the same institution, under the Protocol 670.
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2.1. Database of farmers trained on the FAMACHA© system The study used the database obtained by the project “Training project for small sheep and goat producers to use the FAMACHA© system as an aid in gastrointestinal worm control” (Public Notice 07/2008 from Fundac¸ão Araucária, University Without Frontiers program) performed from July 2009 to May 2011 in the state of Paraná, Brazil. The training program was conducted on two days and consisted of a theoretical session (8 h) and a practical session (2 h). The theoretical session consisted of a workshop addressing the GIN life cycle, parasite resistance, integrated parasite management, and the use of the FAMACHA© system for the selective AH treatment. In the practical session, participants received hands-on training on the use of FAMACHA© including the direct assessment on animals (Maia et al., 2014). During this project, participants completed an application form with personal information, contacts, and professional activity (sheep farmer; goat farmer; farmer of other species; higher degree in agricultural sciences veterinarian, agronomist and animal scientist; agricultural technician; student). 2.2. Post-training questionnaire survey In March 2012, a survey was conducted to describe the GIN control strategies amongst sheep and goats farmers that received the FAMACHA© training course. It also explored the adoption of the FAMACHA© system amongst farmers. For this survey, questionnaires were submitted through electronic mail to all the project trainees. The questionnaire was also sent to city halls and offices of the Department of Agriculture and Food Supply (SEAB), in the towns where the training was held, so that the questionnaire could be distributed to all the participants (1375 people). A total of 1066 electronic questionnaires were sent and 226 questionnaires were provided through local city halls or offices of SEAB. Questionnaires consisted of 15 questions regarding their production system, methods of GIN control as well as their knowledge on parasite resistance. 2.3. Evaluation of FAMACHA© use on farm Participants who classified themselves on the training day as sheep or goat farmers were included in a second evaluation of the use of the FAMACHA© in their own farm. All farmers, even those failing to answer the questionnaire, were contacted by telephone. Those who met the established inclusion criteria were invited to participate in the study by means of in loco visits to their farm. The inclusion criteria were: (a) participating in the whole training, (b) using the FAMACHA© system routinely in their farm, and (c) having more than 20 sheep and/or goats. During the visits, a veterinarian previously trained and experienced in the use of FAMACHA© observed how farmers used the method on their animals. Issues such as animal management (use of crush, individual restraint), the correct exposure of the lower eyelid mucosa, or whether the chart was used or
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not, were assessed. The farmer evaluated 20 animals and, at the end of the assessment, the veterinarian inspected the lower eyelid mucosa of animals correctly applying the FAMACHA© system (Van Wyk and Bath, 2002). Then, the veterinarian collected blood samples for the microhematocrit determination. Blood collection was performed by puncture of the external jugular vein using Vacutainer® tubes with anticoagulant (EDTA). The blood was used to determine the hematocrit value (Ht) as proposed by Jain (1986). At the end of the visit, farmers were interviewed again, with questions regarding satisfaction with the FAMACHA© system, frequency of use, the existence of a record of FAMACHA© scores in the flock, the use of AH and the existence of technical assistance in the farm. 2.4. Statistical analyses The questionnaires of the two stages were tabulated in spreadsheets of the software Microsoft Excel. Univariate and bivariate analysis of answers were performed. Practices adopted for deworming the flocks before and after the training were analyzed by means of respective chi-square tests, with 5% level of significance, using Statgraphics Centurion XVI. FAMACHA© grades assigned by farmers and the hematocrit results of each animal were used to determine sensitivity and specificity values and to observe whether animals were truly anemic, thus, whether the AH treatments were correctly applied. The hematocrit pattern established to confirm anemia, for the sensitivity and specificity tests, was the value ≤18%, since it is the boundary between categories 3 and 4 of the FAMACHA© system (Kaplan et al., 2004). Two criteria were established for calculations: (a) animals classified as FAMACHA© 4 and 5 regarded as anemic, and (b) animals classified as FAMACHA© 3, 4, and 5 regarded as anemic. The sensitivity and specificity values were calculated according to Vatta et al. (2001) and Thrusfield (2005). True positive (TP) were anemic animals identified as such, i.e. animals with hematocrit ≤18% and classified as FAMACHA© 4 and 5, or 3, 4, and 5. True negative (TN) were animals that show no anemia (Ht > 18), i.e. classified as FAMACHA© 1 and 2, or 1, 2, and 3. False positive (FP) values were non-anemic animals with FAMACHA© grades suggestive of anemia. False negative (FN) are anemic animals not identified by the system. When using the FAMACHA© system, sensitivity indicated the proportion of anemic animals correctly identified [SEN = TP × 100/(TP + FN)] and specificity indicated the proportion of non-anemic animals correctly identified [SPE = TN × 100/(TN + FP)]. 3. Results and discussion 3.1. Practices for parasite control From the 1375 people that participated in the training project, a total of 124 people responded the questionnaire totaling 9% of participants. Out of the 124 respondents, 60 (48.4%) were sheep and/or goat farmers, corresponding to 21.3% of farmers trained through the project. Although
farmers represented a smaller proportion of trainees in the project (20.4% of the total), they accounted for nearly half of respondents, which suggests that farmers were more interested in responding to the questionnaire than veterinarians, animal scientists, agriculturalists, agricultural technicians or students. The participation obtained in this study is similar to that found by other workers when applying their questionnaires only to farmers in the UK (McMahon et al., 2013) or the in United States (Merkel and Gipson, 2011). Specific questions were asked to participants who classified themselves as sheep and/or goat farmers. According to the responses obtained from farmers, 83.3% (n = 50) of flocks are aimed at meat production, 10.1% (n = 6) aimed at other purposes such as wool production, research and leisure, followed by 6.6% (n = 4) properties specialized in producing purebreds. Despite the fact that anthelmintic resistance associated with production losses arising from verminosis constitute a major problem for small ruminant production in Paraná and around the world (Kaplan, 2004; Thomaz-Soccol et al., 2004; Papadopoulos, 2008; Kaplan and Vidyashankar, 2012; Torres-Acosta et al., 2012a), only 51.6% of respondents reported losses in their property related to worms. This percentage may be due to non-evident production losses, which are difficult to identify, unlike what happens with death animals. It is difficult for producers to quantify the actual impact of GIN on health and productivity of their animals because these parasites are internal (Torres-Acosta et al., 2012b). Before the training project (considering a total of 58 respondent farmers) mass AH treatment of the entire flock for the control of GIN was performed at regular intervals by 93.1% of the farmers (n = 54). Table 1 shows that AH treatments were applied using the following criteria: (a) monthly treatments (34,5%), (b) when clinical signs of worms were apparent (diarrhea, submandibular edema, low body condition score) (29.3%), (c) according to the management of the flock (breeding season, before birth, at weaning) (27.6%), (c) using FAMACHA© (6.9%). None of the surveyed farmers used the FEC as a criteria for AH treatment. The latter suggests that farmers were not concerned or ignored that such mass treatments lead to the selection of worms resistant to AH drugs. This is consistent with findings in Spain by Rojo-Vázquez and Housking (2013) who reported that approximately a third of producers have no knowledge on anthelmintic resistance in their property, and this fact does not seem to be a main concern. Table 1 also shows that over half of the responding farmers (n = 30; 51.7%) did not know the FAMACHA© system before the training project and 31% (n = 18) claimed to know the system, but did not use it. Poor knowledge and adoption of the system may be related to its recent introduction to this area of Brazil. The first studies were conducted in 2003 and 2004 (Sotomaior et al., 2003; Molento et al., 2004), while the concept of deworming the entire flock to control worms was widely recommended for decades. Furthermore, adopting a new technology, that is more time consuming than mass treatment schemes, is less attractive for farmers and technicians than keeping old practices (Henrioud, 2011). Amongst 17.2% (n = 10) of farmers who claimed to know and use the FAMACHA© system before the
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Table 1 Knowledge on the FAMACHA© system for controlling worms in small ruminants and its use compared to deworming practices applied to the flock before the training course, according to a questionnaire answered by the course participants in the State of Paraná, Brazil. Deworming strategy before the course
Knew FAMACHA© before the course
No
Yes, did not use
Total
Yes, without chart
Yes, photocopy
Yes, purchase chart
Monthly When there were signs of worms According to management Using FAMACHA© According to fecal egg counts Another
11 (19.0%) 11 (19.0%)
4 (6.9%) 6 (10.3%)
4 (6.9%) 0 (0.0%)
1 (1.7%) 0 (0.0%)
0 (0.0%) 0 (0.0%)
20 (34.5%) 17 (29.3%)
6 (10.3%)
8 (13.8%)
1 (1.7%)
0 (0.0%)
1 (1.7%)
16 (27.6%)
1 (1.7%) 0 (0.0%)
0 (0.0%) 0 (0.0%)
3 (5.2%) 0 (0.0%)
0 (0.0%) 0 (0.0%)
0 (0.0%) 0 (0.0%)
4 (6.9%) 0 (0.0%)
1 (1.7%)
0 (0.0%)
0 (0.0%)
0 (0.0%)
0 (0.0%)
1 (1.7%)
Total
30 (51.7%)
18 (31.0%)
8 (13.8%)
1 (1.7%)
1 (1.7%)
58 (100%)
Obs.: all percentages were calculated regarding the total number of answers obtained (58).
training project, most of them did not use the chart during animal assessment (n = 8), and only 1 of the remaining 2 farmers used the official chart (Table 1). Failure to use the FAMACHA© chart as a standard reference of this method (Van Wyk and Bath, 2002) during animal assessments suggest that farmers were exposed to the FAMACHA© system by means failing to provide the chart. The latter is consistent with previous surveys reporting that the main information source for farmers consisted of newspapers, leaflets, pharmaceutical industry, and guidance by other people (Cabaret et al., 2009; McMahon et al., 2013). Before the training project, monthly treatments took place in 34.5% of flocks, and other deworming criteria corresponding to a frequent treatment interval, including treatments every 15 days, every 40 days and bimonthly (Table 1). In the state of Minas Gerais, Brazil, studies involving management practices amongst goat farmers showed that 83% of meat farmers answered to use frequent dewormings in their entire flock, at intervals ranging from 1 month (1–2 months = 48.8%) to more than 4 months
(2.4%) (Guimarães et al., 2011). Similar results were found in sheep flocks in the state of Rio de Janeiro, Brazil, where Cruz et al. (2010) obtained results such as 97% of farmers using dewormings as a way for controlling gastrointestinal worms, the vast majority on a monthly or bimonthly basis (38%). The frequency of AH treatments applied before the training project can be observed in Table 2. Selective treatment was performed by few farmers (20.7%) irrespective of the criteria of treatment used to decide treatment. This indicated that some farmers were already aware of the need to treat only the animals needing treatment. Table 2 also shows that most deworming criteria, concerning which animals were treated, changed after the training (p < 0.0001). Farmers were treating all the animals before the FAMACHA© course (67.2%) and this radically reduced after the course to only 12.1% of farmers. Similarly, the number of people that treated the animals selectively increased from 20.7% to 75.9%. These data suggest again that the course created awareness amongst
Table 2 Practices adopted for deworming flocks before and after the course, regarding the number of small ruminants dewormed, according to a questionnaire sent to participants in the FAMACHA© training course in the State of Paraná, Brazil. Deworming criteria
Which animals Selective
Total All the animals
Per group or category
4 (6.9%) 3 (5.2%) 3 (5.2%) 0 (0.0%) 2 (3.4%) 0 (0.0%)
0 (0.0%) 8 (13.8%) 12 (20.7%) 0 (0.0%) 18 (31.0%) 1 (1.7%)
0 (0.0%) 5 (8.6%) 2 (3.4%) 0 (0.0%) 0 (0.0%) 0 (0.0%)
4 (6.9%) 16 (27.6%) 17 (29.3%) 0 (0.0%) 20 (34.5%) 1 (1.7%)
Total
12 (20.7%)
39 (67.2%)
7 (12.1%)
58 (100%)
After the course Using FAMACHA© According to management When there are signs of worms According to fecal egg counts Monthly
33 (56.9%) 6 (10.3%) 4 (6.9%) 1 (1.7%) 0 (0.0%)
2 (3.4%) 1 (1.7%) 2 (3.4%) 0 (0.0%) 2 (3.4%)
5 (8.6%) 1 (1.7%) 0 (0.0%) 0 (0.0%) 1 (1.7%)
40 (69.0%) 8 (13.8%) 6 (10.3%) 1 (1.7%) 3 (5.2%)
Total
44 (75.9%)
7 (12.1%)
7 (12.1%)
58 (100%)
Before the course Using FAMACHA© According to management When there are signs of worms According to fecal egg counts Monthly Another
Obs.: all percentages were calculated regarding the total number of answers obtained (58).
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farmers that the selective treatment was feasible and desirable. When comparing the deworming methods adopted by farmers before and after the course, it is evident that there was a substantial change (p < 0.0001). After training, 69.0% dewormed according to FAMACHA© . The latter can be considered a great success because only 6.9% of farmers used that technique before the course (Table 2). As a direct consequence, all the other deworming criteria were significantly reduced: (a) monthly treatments was reduced from 34.5% to only in 5.2% of farmers, (b) treatment according to management reduced from 27.6% to 13.8% of farmers and (c) treatments according to signs reduced from 29.3% to 10.3% (p < 0.0001). The level of adoption found in the present study is higher than that reported in previous studies performed in Brazil. In the state of São Paulo, Brazil, 47.1% of flocks surveyed used the FAMACHA© system as a deworming criterion and the signs of worms are taken into account in 41.2% of cases (Veríssimo et al., 2012). On the other hand, Cruz et al. (2010) reported only 3% of FAMACHA© use as a criterion for deworming sheep in Rio de Janeiro. It seems that the higher adoption reported for farmers in Paraná is the result of the FAMACHA© training course. These questionnaire surveys performed in Brazil (São Paulo and Rio de Janeiro) reported the adoption of farmers that did not receive a previous training. Amongst those who did not adopt the system, the main reasons were: (a) time spent for evaluating animals is too long, (b) it is difficult to assess animals by a sole person, and (c) farmers attempt to avoid animal stress. The time constraint has been mentioned as an important reason to resist the adoption of selective anthelmintic treatment schemes, since they require more effort to monitor the flock’s health (Cabaret et al., 2009; Torres-Acosta et al., 2014). The present survey showed that farmers were able to establish a routine to use the FAMACHA© system since 83% of assessments have occurred at monthly intervals or sooner. Meanwhile, around 9.4% of farmers reported that assessments were performed less frequently (from 40 to 90 days). During the training course, the period recommended as ideal was three weeks. Van Wyk and Bath (2002) reported that, for reducing risk of clinical nematodosis in this system, the assessment must be used at short time intervals (from 7 to 14 days), especially during periods with high parasite challenge, corroborating the findings of Burke et al. (2007) and Reynecke et al. (2011). However, a long-term trial testing a targeted selective AH treatment scheme in the tropics of México showed that animal assessments could be performed once every month without evidence of negative consequences for the animals (Torres-Acosta et al., 2014). Finally, up to 7.5% of farmers still reported other criteria to perform the FAMACHA© evaluation (management change and emergency of clinical signs compatible with GIN infection). As for the assessment criterion of the entire flock or a part of it, the FAMACHA© system was applied to all animals in 81.1% of properties. Failing to use it in all the flock seemed to be unrelated to the number of animals (Table 3). At first, there should be no reason for not evaluating all animals, especially in small flocks, such as in most cases in this study. According to Bath et al. (2001), those farms with
sufficient facilities and with experienced personnel allowing, one person who is experienced in the use of the system can inspect more than 500 sheep per hour. For using the FAMACHA© system, recommendations to deworm sheep are always to deworm animals classified as 4 and 5 and in some cases, those classified as 3 (Van Wyk and Bath, 2002). On the other hand, dewormings of goats should always be applied to animals classified as 3, 4, and 5 (Vatta et al., 2001; Van Wyk and Bath, 2002; Mahieu et al., 2007; Sotomaior et al., 2012). According to Table 4, it was observed that 28.3% of dewormings involved only animals classified as 4 and 5. For goats and sheep, the inclusion of deworming in FAMACHA© 3 significantly increases the sensitivity levels of the system (Burke et al., 2007; Reynecke et al., 2011; Sotomaior et al., 2012; Torres-Acosta et al., 2014) but increased the proportion of animals that are supposed to be treated with an AH.
3.2. Use of FAMACHA© by farmers Eight farmers who took part in the theoretical and practical aspects of the FAMACHA© training project were selected for the in loco evaluation. The small number of assessments was due to the difficulty to contact producers. Some farmers were not receptive to sample collection in their property, and, finally, some of them did not have the minimum number of 20 animals. Although all the training participants received the official FAMACHA© chart, its use for evaluating animals was neglected in most cases (87.5%) (Table 5). It is possible that, due to the system’s simplicity, many farmers rely on their memory when evaluating animals. This practice can lead to errors, since colors on the chart are the basis of the FAMACHA© methodology (Bath et al., 2001; Van Wyk and Bath, 2002). During on-farm assessments, farmers fail to provide the correct exposure of animal’s ocular mucosa and they also fail to use the chart. Only 50% of farmers exposed the animal’s ocular mucosa for proper analysis, pressing carefully the upper eyelid and pulling the lower eyelid. The mistake made by the rest of farmers was evaluating with an open upper eyelid. Although farmers were shown how to correctly perform the eye lid and expose the mucosa in their animals, farmers did not practice during training the correct eye opening technique. Thus, it is clear that course participants must practice the correct way of exposing the conjunctival mucosa during the hands-on classes, as indicated by Molento (2009b). Although Kaplan et al. (2004) demonstrated the effectiveness of the use of the system by trained farmers, observed mistakes indicate the need for technical supervision on-farm during a period of “adoption”. The latter suggests that regular calibration (i.e. determination of the relationship between FAMACHA© scoring and the hematocrit gold standard) of the FAMACHA© scoring process amongst trained personnel is essential, since there is a tendency of making mistakes in the classifications (Reynecke et al., 2011). It is important to indicate that, the only case in which errors during training were lower than posttraining, took place in a property that received technical assistance on a monthly basis.
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Table 3 Use of the FAMACHA© system and assessment of the entire flock or a part of it, with regard to the number of animals in the farm, according to the questionnaire sent to participants in the FAMACHA© training course in the State of Paraná, Brazil. Assessment of all animals using FAMACHA©
Number of animals
Yes
Total
Only those that seem to be sick
Less than 20 animals 20–49 animals 50–99 animals 100–499 animals 500–999 animals
17 (32.1%) 7 (13.2%) 9 (17.0%) 9 (17.0%) 1 (1.9%)
2 (3.8%) 5 (9.4%) 1 (1.9%) 2 (3.8%) 0 (0.0%)
19 (35.8%) 12 (22.6%) 10 (18.9%) 11 (20.8%) 1 (1.9%)
Total
43 (81.1%)
10 (18.9%)
53 (100%)
Obs.: all percentages were calculated regarding the total number of answers obtained (58). Table 4 Deworming according to the various grades of FAMACHA© in sheep and goats, according to a questionnaire sent to participants in the FAMACHA© training course, in the State of Paraná, Brazil. FAMACHA© category dewormed
Species of ruminant
Total
4 and 5
4 and 5, in some cases, 3
3, 4, and 5
Sheep Goats Sheep and goats
10 (18.9%) 0 (0.0%) 5 (9.4%)
18 (34.0%) 0 (0.0%) 8 (15.1%)
8 (15.1%) 1 (1.9%) 3 (5.7%)
36 (67.9%) 1 (1.9%) 16 (30.2%)
Total
15 (28.3%)
26 (49.1%)
12 (22.6%)
53 (100%)
Obs.: all percentages were calculated regarding the total number of answers obtained (53).
The absence of a data record system for the FAMACHA© assessments, production and reproductive performance was recorded in 62.5% of properties visited (Table 5). The latter is an important problem as farmers cannot identify those animals recurrently identified with FAMACHA© 4 or 5. This represents a clear disadvantage for farmers, as they cannot eliminate these problematic animals. One advantage of the system is the genetic selection of resistant and resilient animals in the long term (Van Wyk and Bath, 2002; Riley and Van Wyk, 2009), this opportunity was neglected in these cases. Despite the problems mentioned above, the results shown in Table 6 indicated that there were no cases of animals classified as false negatives, i.e. non-anemic animal failing to be dewormed. Producers trained in the United States of America obtained 2.7% of FN assessments, considering Ht ≤ 19 and deworming animals classified as 4 and 5, and 0.6% of FN when animals classified as 3, 4, and 5 were treated (Kaplan et al., 2004). However, there were large numbers of animals receiving unnecessary treatments (FP). Irrespective of the problems mentioned above, the use of the FAMACHA© system is in line with what has been
currently sought for the control gastrointestinal worms, i.e. reducing the number of animals receiving an AH treatment. Providing anthelmintic treatment to 11.9–36.9% of the animals, even when some did not need it, is better than providing treatment to 100% of animals every month. The part of the flock that was not dewormed will contribute to keep the refugia population (Van Wyk, 2001; Van Wyk and Bath, 2002; Kenyon et al., 2009; Besier, 2012). The sensitivity of the system was 100% both, when the deworming of animals level 3 was included, and when only those animals with FAMACHA© 4 and 5 were dewormed. Specificity, however, decreased from 87.8% to 62.42% when FAMACHA© 3 animals were treated. Considering Ht ≤ 19, Kaplan et al. (2004) obtained sensitivity results of 92.2% and 64.1% including and not including the deworming of sheep classified as level 3, respectively. The latter is very similar to the sensitivities (96.9% and 60.9%) reported for goats under tropical conditions by Torres-Acosta et al. (2014), using a Ht < 22. A high sensitivity when using the FAMACHA© system is a desirable factor, because the animals that need deworming do not fail to be treated. Failure to deworm an animal regarded as false negative
Table 5 Data from the farmer’s interviews and the in loco assessment of eight sheep and goat farmers on the use of the FAMACHA© system and property characteristics of farms. Topics evaluated
Number of animals Use of the chart Opens the eye correctly Assessment frequency Recording system Crush Assistance Dewormed
Farmers interviewed and visited A
B
C
D
E
F
G
H
500–999 If in doubt Yes 15 days Yes Yes Monthly 3, 4, 5
50–99 Sometimes Yes 15–30 days Yes No No 2, 3, 4, 5
≤20 Sometimes Yes 60 days No No No 3, 4, 5
≤20 Sometimes Yes 60 days No No No 3, 4, 5
50–99 Yes No 30 days Yes No No 3, 4, 5
100–499 No No When sick No No No 3, 4, 5
20–49 Sometimes No When sick No No No 4, 5
20–49 Sometimes No When sick No No No 4, 5
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Table 6 Values of false negative (FN), false positive (FP), true positive (TP), and true negative (TN) sheep according to the hematocrit value and deworming the animals classed as FAMACHA© 3, 4, and 5 or those classified as 4 and 5 by producers previously trained and evaluated in the state of Paraná, Brazil. Ht
Dewormed
FN
FP
TP
TN
Total
≤18 ≤18
3, 4, and 5 4 and 5
0 0
59 (36.9%) 19 (11.9%)
3 (1.9%) 3 (1.9%)
98 (61.2%) 138 (86.2%)
160 160
may lead to production losses and even death (Vatta et al., 2001; Kaplan et al., 2004).
4. Conclusion People who attended the FAMACHA© training declared that after the course they started to deworm their animals using criteria that could help to maintain a higher proportion of the nematode population in the refugia (that is, untreated) than would be the case if treatment of the whole flock were practised. However, most farmers tended to simplify the FAMACHA© methodology by not using the chart or not keeping a written history of animals dewormed, and half of the farmers had an incorrect technique to expose the ocular mucosa. All these aspects compromise the long-term use of the FAMACHA© system. Errors regarding the use of FAMACHA© on-farm by the trained farmers suggested that training must be improved. Furthermore, there is a need for post-training on-farm monitoring on the correct use of the FAMACHA© system. In spite of the errors detected, farmers detected all anemic animals when evaluated on-farm (100% sensitivity).
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