Pesq. Vet. Bras. 33(4):469-475, abril 2013
Variability in the fecal egg count and the parasitic burden of hair sheep after grazing in nematode infected paddocks1
Roberto González-Garduño2*, Pedro Mendoza-de Gives3 4
ABSTRACT and Glafiro Torres-HernándezVa- riability in the fecal egg count and the parasitic burden of hair sheep after grazing in nematode infected.- González-Garduño paddocks. Pesquisa R., Mendoza-de Veterinária Gives Brasileira P. & Torres-Hernández 33(4):469-475. G.Universidad 2013. Autónoma Chapingo, Unidad Regional Universitaria Sursureste, P.O. Box 29 Teapa, 86800 Tabasco, México. E-mail address: [email protected] This study aimed to evaluate the variability in the fecal egg count (FEC) and the parasi-
was carried out in Tabasco, Mexico, during two periods (August and December). In each periodtic burden 32 lambs of naive were hair grazed sheep for after one grazing month onin nematodeAfrican star infected grass ( Cynodonpaddocks. plectostachyus) The research
and body weight (BW) were recorded. Gastrointestinal worms were recovered at necropsy. Datacontaminated were analyzed with gastrointestinalwith the MIXED procedureparasitic nematodes. of SAS using FEC, a model packed of repeatedcell volume measure (PCV)- ments over time. A higher number of Haemonchus contortus worms was found in Decem- ber (2814±838) than in August (1166±305). The opposite occurred with Cooperia curticei
to the worm burden were higher in December (6516 ± 1599, r=0.83, respectively) than in(2167±393 August (4364±771, and 3638±441, r=0.44, respectively). respectively). The A highFEC variabilityand correlation in resistance-susceptibility coefficient in respect to gastrointestinal nematodes (GIN) occurred in Katahdin × Pelibuey lambs after grazing. INDEX TERMS: Haemonchus contortus, Cooperia curticei, Oesophagostomum columbianum, hair sheep, resistance-susceptibility.
INTRODUCTION control these parasites (Torres-Acosta et al. 2012). Some The frequent and continuous use of chemical anthelmin- strategies to reduce the parasitic burden in the animals have been proposed: selective deworming (Besier et al. presence of lateral and multiple anthelmintic resistance intic thedrugs parasites. for deworming This resistance sheep leadsflocks to has a concerningresulted in inethe- ffectiveness of anthelmintics with large economic losses in al.2010), 2009) vaccination and biological (Arunkumar control (Waller et al. 2006). 2012), medicinal sheep productivity (Coles et al. 2006, Papadopoulos 2008, plantsSelection (Sawleha of sheep et al. 2010), that are cooper genetically oxide needlesresistant (Vatta to gas et- Sargison 2011). Twenty-four countries have reported the trointestinal parasitic nematodes is another possible stra- presence of nematodes resistant to several anthelmintics tegy that has been explored in recent decades (Eady et al. (Jabbar et al. 2006). - - ers around the world to search for alternative strategies to tive has been used in combination with other control me- This situation has motivated work thods,2003, Hutchingsespecially etwhen al. 2007, there Stear is the et problem al. 2007). of anthelminticThis alterna 1 Received on August 3, 2012. drug resistance (Molento 2009). The issue of resistance has Accepted for publication on March 18, 2013. increased mainly for sheep farming in humid, warm clima- 2 Universidad Autónoma Chapingo, Unidad Regional Universitaria Sur- te conditions such as in Brazil (Thomaz-Soccol et al. 2004). sureste, P.O. Box 29 Teapa, 86800 Tabasco, México. *Corresponding au- In these warm, humid areas the proliferation of nematode thor. [email protected] larvae in the grass increases, resulting in the possibility of 3 - larvae completing their biological cycles, thereby creating a ria, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Paseo Centro Cuaunahuac Nacional 8534, de Investigación Progreso, C.P. Disciplinaria 62550. Jiutepec, en Parasitología Morelos, México. Veterina major problem in the grazing sheep industry (Torres-Acos- 4 Colegio de Postgraduados, Programa de Ganadería, Instituto de Re- cursos Genéticos y Productividad, 56230 Montecillo, Estado de México. The genetic selection of sheep resistant to nematodes México. ta & Hoste 2008). -
is based on phenotypic markers. For example, the elimi 469 470
Roberto González-Garduño, Pedro Mendoza-de Gives and Glafiro Torres-Hernández nation of eggs per g of feces in wool sheep breeds has been investigated for many years in Australia and New Zealand (Windon 1996, Gray 1997). In Merino, there are lines of sheep selected for both increased and reduced genetic re- sistance (Woolaston et al. 1990). These lines achieve ave- possible to reduce the use of anthelmintics in controlling nematodesrage counts in of sheep 2730 andwith 17400 genetic epg, resistance. respectively, The searchmaking for it genes or Quantitative Trait Loci (QTL) related to resistan- ce against parasites in sheep is considered a major aspect countries, i.e. UK (Davies et al. 2006, Bishop & Morris 2007) andto be Kenya investigated (Silva et (Beraldi al. 2012). et al. Despite 2007) theby workers development in some of Fig.1. Rainfall and temperature averages from 1971 to 2000 re- modern molecular techniques, traditional productive as- corded at the Meteorological Center, 27068 Puyacatengo, Ta- basco, Mexico. et al. 2004) and egg faecal count have been used to diagno- sispects parasites such as (Cringoli weight gain, et al. packed 2010). cell volume (Vanimisetti The study was divided into two periods. In each period, 32 Studies indicate that hair breeds are more resistant to Katahdin × Pelibuey three- month-old weaned male lambs were parasitic nematodes than wool breeds. For instance, in a used. The lambs of each period had never been in contact with GIN because they were reared in house with ewes during the pre- - weaning period. At weaning, they were negative to gastrointes- tinal nematodes; consequently, no acquired resistance against work published by Notter et al. (2003), authors recorded bs. Meanwhile, in hair lambs maintained under the same nematodes would be expected. conditions,4011 FEC average only 1135 after FEC four was to found.eight weeks On the in other wool hand, lam lambs were grazed for one month in a rotational system with 15 gastrointestinal parasitic nematodes with values of 5170 daysThe grazing first periodin each wasone ofcarried two 7500m out in2 August (rainy season) and Katahdin and St Croix have been identified as resistant to lambs were given 250g of a commercial feed with 14% crude pro- Miller 2004). Also, one hair sheep breed from the Canary tein. Also, they were provided with a mineral paddocks. mixture During and grazing, water Islandsand 4217 (Canaria FEC and hair Dorper breed lambs sheep) with (González 8602 FEC et (Burkeal. 2008) & ad libitum. After grazing, lambs were housed for 21 days to allow and another from Mexico (Pelibuey) are also recorded as the larvae to evolve into adult worms. Lambs from this group resistant against gastrointestinal nematodes (Morteo-Gó- were slaughtered to recover the nematode parasites. mez et al. 2004). Other studies also indicated the presence 38 infected sheep were grazed on the pastures for three months of resistance in the following breeds: Florida (Amarante et fromAfter September completing to November the first grazing (rainy season)period, anto continuously“extra” group in of- al. 1999, Díaz et al. 2000), Gulf Coast native (Li et al. 2001), fect the prairie with gastrointestinal nematodes. In the second period, another group of 32 grazing lambs with the same characteristics, origin and management, previously indi- BlackbellyThe high (Amount variability et al.observed 2003), betweenRed Maasai and (Baker within et bre al.- cated, was introduced. This group grazed for a month (December) eds2003) allows and Dorperfor selection (Vannimiseti based on et theal. 2004). nematode egg count and was then housed for 21 days. The January group was slau- despite the heritability and repeatability being close to 0.3 ghtered to recover the nematode parasites. Individual body weight (BW) was recorded at the beginning alternative for controlling parasitic nematodes. The aim of and at days 35 and 42 of each period, and the average daily wei- the(Jackson present 2002). study Nevertheless, was to identify it should the variabilitybe considered between as an ght gain (DWG) was estimated. On the same dates, blood samples the fecal egg count and the parasitic burden of hair sheep - were taken from the jugular vein to measure the packed cell volu Parasitologicalme (PCV) by the micro-haematocrit method technique (Benjamin 1991). after grazing MATERIALSin nematode infected AND METHODS grazing paddocks. Experimental site This study was carried out in the Unidad Regional Universita- 21, During35 and grazing,42. The fecalMcMaster samples technique were taken was onused days to determine14, 21, 35 ria Sursureste of the Universidad Autónoma Chapingo in the Muni- theand FEC 42. valuesDuring (Thienpont the housing et period,al. 1986). samples Fecal samples were taken were on pooled days cipality of Teapa, Tabasco, Mexico, at 60 meters above sea level and and then cultured to obtain nematode infective larvae for taxono- located 17° 31’ 38” North latitude and 92° 55’ 50” West longitude. The prevalent climate of this region is Af (m) wi’g, hot and humid At the end of the housing time in each period, lambs were with rainfall throughout the year (Fig.1). The average annual tem- mic identification (Niec 1968). perature is 25.8ºC and rainfall of 3976mm (CONAGUA, 2012). ZOO-1995 for humanitarian slaughter of domestic animals and wildlifeslaughtered (SENASICA, according 1996). to the After Mexican slaughter, Official the Standard abomasum NOM-033- of each Animals and management lamb was removed and dissected as follows: The organ was ope- The grassland was planted with African star grass (Cynodon ned along the greater curvature and the content was collected in a plectostachyus) nine months before starting the experiment. plastic container and then the worms were recovered. At the same Three months before the lambs began the grazing period, one time, worms were recovered from the intestinal tract and also group of 40 sheep was grazed on this prairie in order to contami- from distal part of the colon and rectum. At the same sampling nate it with GIN. time, 10% formalin was added to preserve the recovered parasi-
Pesq. Vet. Bras. 33(4):469-475, abril 2013 Variability in the fecal egg count and the parasitic burden of hair sheep after grazing in nematode infected paddocks 471 tes. The content of the abomasum, colon and rectum was washed Table 2. Relative frequency of worm burdens in the with tap water and passed through a mesh (Mesh number 50, gastrointestinal tract of sheep grazing during two 0.297mm, Mont-steel) and content of small intestine was washed study periods and meshed through a mesh number 400 (0.038mm, Mont-steel). Classes Classes mean Accumulate relative frequency (%) Finally, the content and parasites retained in the mesh were col- Lower Upper value First period Second period limit limit (September) (January) including males and females from aliquots, were mounted on sli- deslected and in observed a 500 mL under flask a(Tarazona microscope 1973). (10X Recovered and 40X) for nematodes, the taxo- 30 1515 772 9.7 31.0 Jacquiet et al. 1997). 1515 3000 2257 35.5 55.2 3000 4485 3742 45.2 65.5 4485 5969 5227 58.1 72.4 Statisticalnomic identification analysis (Vázquez 1989, 5969 7454 6712 80.6 75.9 Least square means and standard errors were estimated from 7454 8939 8197 96.8 79.3 repeated measure analysis of variance (SAS 1999). FEC was trans- 8939 10424 9682 100.0 86.2 a formed to log10 (FEC + 25) to correct the heterogeneity of variance 10424 16364 13394 89.7 and to obtain a normal distribution approximation of data follo- 16364 17848 17106 93.1 wing the method of Gauly & Erhardt (2001). 17848 19333 18591 100.0 a Four classes were grouped. The following model was used: Y =m + e i j(i) Similar averages in the worm burdens in both periods ijk + ρ + α + τk(i) ijk - Where: Y μ i ~ N wever, there were differences in the count of each spe- j(i) ijk j(i) 2 is the FEC, PCV or DWG, the mean,2 ρ the fixed effect of (0, s a Fixed effect of the time, e ~ N (0, s e) the residual error. cies(4989 per y period. 4832 worms, There were respectively) more H. contortus were observed. in January Ho period, α the random effect of j-esim animal in the i-esim period α k(i) ijk (2814±838) than in September (1166±305). The opposi- ). τ The results of counting the recovered worm species (Haemon- te situation occurred with C. curticei (Table 3); the lambs chus contortus, Cooperia curticei and Oesophagostomum colombia- slaughtered in September had 3638±441 nematodes of num) and the total worm burdens were log + 25 transformed and analyzed using the same model, but removing the effect of time. One frequency table was performed to determine the dispersion the count worms found in lambs slaughtered in January (2167this species±393). In (p≤0.05) the case which of O. columbianum was a higher, the number lambs slau than- class interval 1500 nematodes with the purpose of forming more ghtered in September had more worms (68±25) of this spe- thanof nematode 6 classes. counts The incorrelation the group ofanalyzes lambs in were each performed period, taking using as the CORR procedure among the study variables with SAS software in January (9±4). (SAS 1999) and scatter plots and trend lines in Excel. ciesThere compared were to differences those recovered in fecal from egg thecounts lambs between sacrificed pe-
RESULTS period (December, 6516±1599 EPG) compared with the The total count of recovered parasites at necropsy was riods (P≤0.01). Higher±771). FEC The values highest were FEC found values in were the last re- 4908 ± 4405 for all experiment. This count included a mix- corded at day 21 during the second period (Fig.2). ture of species conformed by Haemonchus contortus, Coo- first (August, 4364 peria curticei and Oesophagostomum columbianum initially - thanThe in thecorrelation second period coefficient (r=0.83). between This thecoincided worm burdenswith the logic measurements of nematode males (Table 1). highestand fecal number egg counts of H. incontortus the first found period during (r= 0.44) the lastwas period lower identifiedOnly one in thelamb coprocultures in each of the and two determined periods had by a morphovery low Table 3. Average and standard error of worm burdens in Katahdin x Pelibuey sheep during two periods - riodworm and burden 30% in(20 the in secondthe first period period had and the 30 lowest in the second).parasite Species and sex First period Second period burdenApart from (1500 these worms). animals, On 10% the otherof the hand,lambs 3%in the of firstthe ani pe- (September) (January) Worm count Worm count N* Average Std Error N* Average Std Error about 20% in the second period exceeded this number of nematodesmals had more (Table than 2). 7500 worms in the first period while Haemonchus contortus Females 30 673b 185 29 1529ª 446 Males 30 494b 127 29 1285ª 395 Table 1. Morphometry of the adult male nematode species Total 30 1166b 305 29 2814ª 838 found in the gastrointestinal tract of sheep Cooperia curticei Females 30 1994ª 219 29 1171b 207 a Specie Location N Body length Spicules (µm) Males 30 1643ª 233 29 996b 187 (mm) Right Left Total 30 3638ª 441 29 2167b 393 H. contortus Abomasum 48 13.36 ± 1.7 39.8 ± 2.7b 21.0 ± 1.7b Oesophagostomum columbianum b O. columbianum Intestine 10 13.5 800 ± 25.0 800 ± 25.0 Females 30 38ª 14 29 3 1 b C. curticei Small intestine 20 c 153.0 ± 13.0 153.0 ±13.0 Males 30 30ª 11 29 6 3 Total 30 68ª 25 29 9b 4 a N = Number of nematodes. b - Total 30 4832ª 492 29 4989ª 1053 res were 407.6 ± 15.3. c Measures of the hooks; the spicules measu- ab malin and rolled. *N = Number of sheep. There was no measurement of the body because they were fixed in for Different letters in each row indicate statistical differences (p≤0.01).
Pesq. Vet. Bras. 33(4):469-475, abril 2013 472
Roberto González-Garduño, Pedro Mendoza-de Gives and Glafiro Torres-Hernández Table 6. Percentage of packed cell volume and body weight per period in Katahdin x Pelibuey sheep Day and period Body weight N Average Std dev Average Std dev Packed cell volume First period 1 31 28.8 2.7 19.4 4.0 35 31 28.6 3.9 19.0 4.1 42 30 26.7 3.6 20.2 4.2 Second period 1 32 33.5 2.3 21.4 5.7 21 31 27.7 3.8 35 30 23.9 4.8 21.1 5.2 42 30 25.6 5.9 22.2 5.5
Table 7. Correlation coefficients between the worm burden, fecal egg count (FEC), change in packed cell volume (PCV) and Fig.2. Fecal egg counts of gastrointestinal nematodes per period daily weight gain (DWG) of sheep in the first period (above and sampling date in Kathadin x Pelibuey lambs. the diagonal) and the second period (below the diagonal)
- First period Variable Worm count FEC PCV change DWG tween the worm count of this species and fecal egg counts Worm count 1 0.44* -0.44* -0.38* (Tableand whose 4). The correlation fecal egg count coefficient and the was worm high burdens (r=0.91) had be a FECa 0.83** 1 -0.56** -0.91** greater tendency after 42 days of infection (Table 5). -0.78** -0.77** 1 0.55** period Second DWG -0.67** -0.68** 0.81** 1 PCV change lambs became infected and the fall was more pronounced ns in theThe second PCV of period lambs (December,in the two periodsTable 6). decreased The largest as there- was* P≤0.05; lower ** P≤0.001; and less P≥0.05. adjusted to the total count of worms in highest number of H. contortus and with high FEC. There- the gastrointestinal tract (R2=60%). duction in PCV in the second period also coincided with the The BW of the lambs fell in the initial samples and then worm burden were negative in both periods (Table 7). increased (Table 6). In DWG differences were found betwe- fore,The the high correlation worm burdens coefficients coincided between with the the PCV decrease and the in was lower than the second period and the most important (R2= 60%) during the second period when there was a larger changesen the two were periods observed (p≤0.05). over time. The DWG in the first period numberPCV values of H.and contortus showed a linear trend which had the best fit DISCUSSION Table 4. Correlation coefficients. In the first of fecalperiod, egg PCV counts reduction and worm burdens of Haemonchus contortus and Cooperia curticei in the first period (above the diagonal) and second burden indicates that a wide variability exists in the innate period (below the diagonal) resistance-susceptibilityThe high coefficient of variation of a contemporary (93%) found group in the of worm hair sheep against gastrointestinal nematodes. The worm bur- FEC H. contortus C. curticei count worms worms dens observed in this study (30 to 19333) were similar to Variable Worm values found (from 7364 to about 19193) in grazing sheep First period Worm count 1 0.44* 0.44* 0.80** (Uriarte et al. 2003). The wide variation among hosts has FECa 0.83** 1 0.86** -0.09ns Teladorsargia circumcincta parasit- H. contortus worms 0.94** 0.91** 1 -0.18ns ized sheep. This variability has also been widely recognized ns Second period C. curticei worms 0.68** 0.29 0.38* 1 also been identified in a ns and has been attributed to differences in the ingestion of in- fectiveamong larvaeand within and the breeds immune (Dominik response 2005, (Stear Idris et et al.al. 2007).2012) Table Fecal egg 5. Trendcounts (eggs among per fecalgram ofcounts feces). of* P≤0.05; nematode ** P≤0.001; eggs (x) P≥0.05. and - the number of worms (Y) found in the gastrointestinal tract tween FEC and worm burdens was smaller (r=0.44) than in mixed infections of Haemonchus contortus and Cooperia During the first period, the correlation coefficient be curticei the one recorded in the second period (r=0.83). The cor- relation was the result of lower FEC recorded in August Days after Worm count Female worm count (4363) due to the lowest number of adult worms of H. con- 2 2 infection equation R equation R tortus (1166) and high counts of Cooperia curticei (3638). First perioda In December the highest FEC (6516) coincided with the 35 Y = 1509 x0.153 0.16 Y = 868 x0.15 0.16 high number of specimens of Haemonchus contortus (2814) 42 Y = 264.6 x0.339 0.47 Y = 161.7x0.329 0.45 Second period and the smallest number of C. curticei (2167). In a similar 21 Y = 199.3x0.437 0.44 Y=120.7x0.422 0.42 case, a high correlation between worm burdens and FEC 35 Y = -5*10-6x2+0.544x+2056 0.58 Y =-3*10-6x2+0.303x+1108 0.58 (0.64 to 0.73) in Rhön sheep infected with H. contortus was 42 Y = -2*10-6x2+0.412x+1659 0.75 Y =-1*10-6x2+0.230x+891.1 0.75 recorded (Gauly et al. 2002). Also, a high correlation (0.85 a On day 21 the FEC was 0. to 0.91) between pre-slaughter FEC and total trichostron-
Pesq. Vet. Bras. 33(4):469-475, abril 2013 Variability in the fecal egg count and the parasitic burden of hair sheep after grazing in nematode infected paddocks 473
using the same methodology. An abundance of C. curticei et al. 1996). It is noteworthy that in the case of a mixed in- in this area was observed in both the rainy season and in fectiongyle burdens (H. contortus in Romney and lambsC. curticei has) been the correlation identified (Bissetvalues were dependent on the abundance of H. contortus (r=0.86 H. contortus inwinter January (Vasquez compared et al. with 2006). September, A previous October study and in Tabasco, Novem- than those of C. curticei ber.Mexico, This also study confirms found the abundance higher prevalence of C. curticei of in July and in the first period and r=0.91 in the second period) rather August (González-Garduño et al. 2011). (R= -0.09 in the first period and- In this study the negative relationship between the FEC r=0.29 in the second period; not significant). factorsAs noted such inas thethe studyabundance of Amarante of each (2000), species with and fieldthe ovi in- - positionfections therate FEC become does important. not reflect Inparasitic the case burdens. of H. contortus Other and PCV was clear. This behavior is also reported in other the oviposition rate is very high, ranging between 5000- breeds such as Dorset, Dorper and Kathadin by Vannimi 10000 eggs per day per female worm (Coyne et al. 1991, valuessetti et were al. (2004), observed who in foundRhön sheep. correlation A correlation coefficients ran of- Romero & Boero, 2001). Whereas for the case of C. curticei, ge-0.46 of r=between -0.21 to PCV -0.34 and (Gauly FEC. In & other Erhardt studies, 2001, PCV Gauly and et FEC al. studies have reported a rate of 20 to 60 eggs and low values 2002), which was lower than those observed in the present of correlation between the FEC and total worms (Amarante study, was found. This can probably be explained because 2000). It is also important to consider the immunological effect of lambs. In this regard, some studies have shown that theseAs authorsexpected, evaluated weight gain, only worm the PCV burdens values. and In theFEC present are re- lambs can not only effectively limit worm establishment, study our information included the change in PCV levels. but can also suppress fecundity of those worms which do situation has already been stated in general terms in other manage to establish (Bisset et al. 1996). The correlation versed with negative correlation coefficients (Table 7). This observed between adult worm size and egg content leads The low initial DWG was due to the drastic change of to the hypothesis that egg production in H. contortus is li- breeds with smaller values (r= -0.25; Vanimisetti et al. 2004). mited by immune regulation of worm size and presumably similar situation occurred in the second period. The BW growth. Mean worm size and fecundity declined as sheep offood the system lambs fromfell in confinementthe initial samples to grazing and then of all increased sheep. A - perhaps as a result of management that was provided. For - received more prolonged trickle infections before necrop pplemented with 250g of commercial food and were hou- 2002,sy, confirming Rowe et al.that 2008). immune responses to adult worms are sedexample, with adduring libitum the food first the month following of grazing, 21 days. lambs were su enhancedThe relation by ongoing between larval FEC challenge and worm (Valderrabano burden had a et bet al.- These results showed that Katahdin x Pelibuey sheep had a high variation in resistance-susceptibility to gastroin- is about 15-28 days (Romero & Boero 2001) and on day 21 testinal parasitic nematodes and at least 3% of the animals manyter fit afteranimals 35 dayshad infectionnot excreted because eggs. the Therefore, pre-patent the period FEC showed high resistance to nematode parasitic burden. does not correlate well with worm count, while on days 35 Fecal egg count may be a suitable indicator to estima- te the number of H. contortus - welland 42following the curves natural are fitted challenge over 50%.in Romney In the lambssame manner (Bisset and the total number of C. curticei since was the not correlation a good indicator coeffi etas al.in the1996). present study, the first egg counts did not correlate forcients mixed were infections. high. However, the relationship between FEC A greater number of lambs with high worm burdens in the second period could be explained by the increase in in- REFERENCES fection of pastures once the number of grazing cycles had - Bazer F.W. 1999. Comparison of naturally acquired parasite burdens Amarante A.F.T., Craig T.M., Ramsey W.S., El-Sayed N.M., Desouki A.Y. & been increased. In the first period (September) lambs gra 85:61-69. among Florida Native, Rambouillet and crossbreed ewes. Vet. Parasitol. zed on paddocks previously infected during three months Amarante A.F.T. 2000. Relationship between faecal egg count and total months;by one flock. therefore, The lambs there in were the second more cyclesperiod of grazed infection on the in worm counts in sheep infected with gastrointestinal nematodes. Braz. thesame pasture. paddocks So, inmore which generations other flocks of parasitesgrazed for were three conta more- J. Vet. Parasitol. 9(1):45-50. - analysis on serum antibody levels of sheep immunized with crude ex- ded in Spain and they are considered as a cause of increased Arunkumar S., Basith A.S. & Gomathinayagam S. 2012. A Haemonchus comparative minating such paddocks. Similar results have been recor- contortus. ver, environmental conditions could also affect the amount tract and thiol-purified excretory/secretory antigen of Vet. World. 5(5):279-284. ofinfection parasites in presentAragonesa in the sheep pasture. (Uriarte During et al. the 2003). months Howe from to sympatric and allopatric isolates of Haemonchus contortus September to December, the moisture increases in the re- Aumont G., Gruner L. & Hostache G. 2003. Comparison of the resistance Parasitol. 116:139-150. of Black gion (Fig.1). Therefore, the environmental conditions lead Belly sheep in Guadeloupe (FWI) and of INRA 401 sheep in France. Vet. E.O. & Thorpe W. 2003. Resistance and resilience to gastro-intestinal The high frequency of H. contortus in the study area was Bakernematode R.L., Nagda parasites S., Rodríguez-Zas and relationships S.L., withSouthey productivity B.R., Audho of Red J.O., Maasai, Aduda reportedto increase in the previous nematode studies. populations This frequency (Eysker et was al. 2005).deter- Dorper and Red Maasai x Dorper crossbred lambs in the sub-humid tro- mined through fecal culture (González et al. 2003) and by pics. Anim. Sci. 76:119-136.
Pesq. Vet. Bras. 33(4):469-475, abril 2013 474
Roberto González-Garduño, Pedro Mendoza-de Gives and Glafiro Torres-Hernández - - musa, México. 421p. -de Gives P. & Arece-García J. 2011. Prevalencia de parásitos gastroin- Benjamin M.M. 1991. Manual de Patología Clínica en Veterinaria. Ed. Li González-Garduño R., Torres-Hernández G., Córdova-Pérez C., Mendoza Pemberton J.M. 2007. Quantitative trait loci (QTL) mapping of resistan- Méx. 42(2):125-135. Beraldice to strongylesD., McRae A.F.,and coccidiaGratten J.,in Pilkingtonthe free-living J.G., SoaySlate sheepJ., Visscher (Ovis P.M.aries &). Graytestinales G.D. 1997. en ovinosThe use sacrificados of genetically en resistant un rastro sheep de Tabasco, to control México. nematode Vet. Int. J. Parasitol. 37:121-129.
treatment approach for effective and sustainable sheep worm manage- resistantparasitism. sheep Vet. Parasitol.avoid parasites 72:345-366. to a greater extent than do susceptible Besierment: R.B., investigations Love R.A., Lyonin Western J. & Van Australia. Burgel Anim.A.J. 2010. Prod. A Sci. targeted 50:1034-1042. selective Hutchingssheep. Proc. M.R., R. Knowler Soc. B 1620:1839-1844. K.J., McAnulty R. & McEwan J.C. 2007. Genetically Bishop S.C. & Morris C.A. 2007. Genetics of disease resistance in sheep and Idris A., Moors E., Sohnrey B. & Gauly M. 2012. Gastrointestinal nematode goats. Small Rum. Res. 70:48-59. infections in German sheep. Parasitol. Res. 110:1453-1459. Jabbar A., Iqbal Z., Kerboeuf D., Muhammad G., Khan M.N. & Afaq M. 2006. Nematode burdens and immunological responses following natural Anthelmintic resistance: the state of play revisited. Life Sci. 79:2413- Bissetchallenge S.A., Vlassoff in Romney A., Douch lambs P.G.C., selectively Jonas bredW.E., forWest low C.J. or & high Green faecal R.S. worm1996. 2431. p.103-107. In: - Torres A.J.F. & Aguilar C.A.J. (Eds), 2º Curso Internacional del Epidemio- egg count. Vet. Parasitol. 61:249-263. tode parasites in Dorper, Katahdin, and St. Croix lambs under conditions Jacksonlogía y F. Control 2002. Selección Integral degenética Nematodos en pequeños Gastrointestinales rumiantes, de Importan- Burkeencountered J.M. & Miller in the J.E. southeastern 2004. Relative region resistance of the Unitedto gastrointestinal States. Small nema Rum. cia Económica en Pequeños Rumiantes. Fundación Produce Yucatán A.C. Res. 54:43-51. Mérida, Yuc. - Hae- monchus species in domestic ruminants based on morphometrics of Coles G.C., Jackson F., Pomroy W.E., Prichard R.K., von Samson-Himmels Jacquietspicules. P., Parasit.Cabaret Res. J., Cheikh 83:82-86. D. & Thiam E. 1997. Identification of tjerna G., Silvestre A., Taylor M.A. & Vercruysse J. 2006. The detection Parasitol. 136:167-185. - CONAGUA.of anthelmintic 2012. Servicioresistance Meteorológico in nematodes Nacional. of veterinary Normales importance. climatológi Vet.- - Li Y., Miller J.E. & Franke D.E. 2001. Epidemiological observations and he Molentoterosis M.B.analysis 2009. of gastrointestinalParasite control nematode in the age parasitism of drug resistancein Suffolk, Gulfand 2012.cas de la estación 27068 Puyacatengo
- mintiasis por Medio del Examen Coprológico. Janssen Research Founda- of hair sheep composite breeds: Resistance of lambs to Haemonchus Thienponttion, Beerse, D., Rochette Bélgica. 205p.F. & Vanparijs O.F.J. 1986. Diagnóstico de las Hel Vanimisetticontortus . H.B.,J. Anim. Greiner Sci. 82:595-604. S.P., Zajac A.M. & Notter D.R. 2004. Performance - - 2006. Comparación de dos sistemas de pastoreo en la infestación con Thomaz-Soccoltestinal nematodes V., Pohl to de anthelmintics Souza F., Sotomaior in sheep C., Alcântara(Ovis aries Castro). Braz. E., Arch. Mil Vásquez H.M., González G.R., Torres H.G., Mendoza de G.P. & Ruiz R.J.M. czewski V., Mocelin G. & Pessoa e Silva M. 2004. Resistance of gastroin The potential to con- S1516-89132004000100006 trolnematodos Haemonchus gastrointestinales contortus in indigenousen ovinos de South pelo. African Vet. Méx. goats 37:15-27. with cop- Biol. Technol. 47(1):41-47. (Online) [Cited 2013-02-26]. Doi: 10.1590/ Vatta F.A., Waller J.P., Githiori B.J. & Medley F.G. 2009. limit gastro-intestinal parasitism in grazing sheep and goats. Small Rum. Torres-AcostaRes. 77:159-173. J.F.J. & Hoste H. 2008. Alternative or improved methods to gastroentéricoper oxide wire particles.de rumiantes, Vet. Parasitol.p.72-82. In: 162(3/4):306-313. Campos R. & Bautista G. (Eds), Torres-Acosta J.F.J., Molento M. & Mendoza de Gives P. 2012. Research and Vázquez P.V.M. 1989. Necropsia e identificación de helmintos del tracto implementation of novel approaches for the control of nematode parasi- WallerDiagnóstico P.J. 2006. de Sustainable Helmintos nematodey Hemoparásitos parasite de control Rumiantes. strategies Asociación for ru- Mexicana de Parasitología Veterinaria, Jiutepec, Morelos, México. tes in Latin America and the Caribbean: Is there sufficient incentive for a - greater extension effort? Vet. Parasitol. 186:132-142. trointestinal nematode burden in sheep under an intensive grazing sys- minant livestock by grazing management and biological control. Anim. Uriarte J., Llorente M.M. & Valderrábano J. 2003. Seasonal changes of gas Immunol.Feed Sci. Tech. lmmunopathol 126(3/4):277-289.. 54:245-254. WoolastonWindon R.G. R.R., 1996. Barger Genetic I.A. control & Piper of L.R.resistance 1990. toResponse helminths to inhelminth sheep. Vet. in- tem. Vet. Parasitol. 118:79-92. fection of sheep selected for resistance to Haemonchus contortus. Int. J. ValderrábanoParasitol. 104:327-338. J., Delfa R. & Uriarte J. 2002. Effect of level of feed intake on Parasitol. 20(8):1015-1018. the development of gastrointestinal parasitism in growing lambs. Vet.
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