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The spread of porcine sarcoptic mange during the fattening period revealed by development of antibodies to Sarcoptes scabiei
veterinary parasitology ELSEVIER
Veterinary Parasitology 73 (1997) 315-324
The spread of porcine sarcoptic mange during the fattening period revealed by development of antibodies to Sarcoptes scabiei Per Wallgren a,*, Set Bornstein b a Department of Ruminant and Porcine Diseases, National Veterinary Institute, Box 7073, 750 07 Uppsala, Sweden b Department of Parasitology, National Veterinary Institute, Box 7073, 750 07 Uppsala, Sweden
Received 12 February 1997; accepted 29 May 1997
Abstract Using an indirect ELISA based on a whole body homogenate of Sarcoptes scabiei var vulpes, the development of serum antibodies to S. scabiei var suis during the fattening period was studied in two herds, purchasing fatteners and performing age segregated production systems. All the pigs in one of the herds were treated with ivermectin on the same day within a week after arrival, while no precautions were made to prevent sarcoptic mange in the other herd. In both herds, a transient immune response to S. scabiei was detected in some animals during the early fattening period, reflecting that these pigs had been exposed to S. scabiei before delivery to the fattening units. It also indicated that they had been treated with acaricides close to allocation. The incidence of animals seropositive to S. scabiei was initially low in both herds. The infection spread gradually as indicated by increasing optical densities of antibodies to S. scabiei, especially during the second half of the rearing period. This increase was more pronounced in the herd which had received no prophylactic treatment to sarcoptic mange. The infection with S. scabiei was found to have spread to more animals towards the end of the fattening period in that herd. It was concluded that a single injection with the acaricide on arrival at the fattening farm decreased and delayed the spread of the infection, but did not eradicate the mite infection. The results showed that conventional pigs sold as fatteners at present may be infected with S. scabiei and that precautions aimed at preventing sarcoptic mange therefore, are indicated in fattening herds. In this context, the ELISA employed could be a valuable means of discriminating between S. scabiei var suis infected piglet producing herds and uninfected herds. © 1997 Elsevier Science B.V. Kew,ords: Pig-Arthropoda; Sarcoptes scabiei; Mange; Immune response-arthropoda; Fatteners; Epidemiology
* Corresponding author. Tel.: +46-18-674000; fax: +46-18-309162. 0304-4017/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PII S0304-4017(97)001 18-0
316
P. Wallgren, S. Bornstein / Veterina O' Parasitology 73 (1997) 315-,¢24
1. Introduction
One of the most economically significant parasitic diseases within modem pig production is sarcoptic mange, caused by the itch mite Sarcoptes scabiei vat suis (Dobson and Davies, 1992). S. scabiei infections cause the swine industry substantial economic losses. According to previously published reports, an infected sow in USA will cost 84-115 US dollars annually due to decreased productivity (Gaafar et al., 1986; Arends et al., 1990). The prevalence of sarcoptic mange is reported to vary from 20 to over 90% within swine populations and 70 to 90% of the herds are reported to be infected with S. scabiei (Dobson and Davies, 1992; Guit~rrez et al., 1996). Although there are effective acaricides available and although these drugs are used in large quantities both prophylactically and therapeutically, high prevalence of S. scabiei infection is still common. The generally recommended and often employed management practice of prophylactically treating herds for sarcoptic mange, (e.g., acaricidal treatment of sows 1-4 weeks prior to farrowing or treatment on herd basis once every 6-12 months), does not eradicate S. scabiei from swine herds. Instead, such programmes often reduce the degree of infection in the herds to subclinical rates. Thus, the infection is maintained on a herd basis and some animals remain as carriers of the mites (Bogatko, 1974). Pig fattening enterprises, which buy pigs at 22-25 kg body weight from several different piglet producers are continuously confronted with the risk of introducing S. scabiei infections into their herds. In this context it should be clarified that the all in-all out production system in itself does not give protection against the disease since these herds are repeatedly restocked through purchase of pigs of unknown status regarding S. scabiei (as well as other infections). Therefore, several farm managers have applied acaricidal treatment to all their animals at the time of restocking in order to prevent the development of sarcoptic mange (Palm6r, 1989). The aim of this work was to study whether infections with S. scabiei occur in specialised fattening herds employing age segregated rearing systems. For this purpose S. scabiei antibody detection by an indirect ELISA was employed in two herds throughout the fattening period. In one of the herds, precautions aimed at combating sarcoptic mange were performed, while no such efforts were made in the other herd.
2. Materials and methods 2.1. Herds and experimental design
Two specialised fattening herds, rearing pigs from 25 to 107 kg live body weight, were chosen for the study. Both herds consisted of a single unit and applied the all in-all out production system. Herd A housed 485 pigs in 62 pens located in lbur rows and herd B housed 220 pigs in 22 pens located in two rows. In both herds, straw was provided daily. The lying area of the pens had solid floors, while the dunging areas
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consisted of slatted floors. Nose to nose contacts with pigs in adjacent pens in the same row as well as with pigs in facing pens on the opposite side of the dunging area were possible through the fences of the pens. To prevent sarcoptic mange, all pigs in herd A were injected subcutaneously with l0 mg ivermectin (Ivomec, MSD, Rahway, U S A ) during the first week after arrival at the herd. In herd B, no precautions against sarcoptic mange were taken. In both herds, four pigs from each of the 10 pens were randomly chosen for the study. These pigs were repeatedly blood sampled by jugular vein punctures using evacuated glass tubes without additives (Becton Dickinsson, Meylan Cedes, France) every third week during the rearing period (i.e., during week 0, 3, 6, 9, 12 and 15). The pens housing the sampled pigs were evenly distributed within the fattening units.
2.2. Detection o f antibodies to Sarcoptes scabiei
Antibodies to S. scabiei were estimated by an indirect E L I S A earlier described (Bornstein and Zakrisson, 1993; Bornstein and Wallgren, 1997). In brief, duplicates of sera diluted 1 / 2 0 0 were analyzed in microtiter plates (Greiner labortechnik, Frickenhausen, Germany) coated with a whole body homogenate of S. scabiei var vulpes diluted in 0.1 M carbonate buffer (pH 9.6). On each microtiter plate, positive and negative controls were employed and the optical density of each plate was corrected to a value of A492 = 1.05 for the positive control sera. The cut-off value lbr samples tested was previously defined as A492 >_ 0.175, corresponding to the mean value plus 3 S.D. of SPF sows (Bornstein and Wallgren, 1997).
density
0.3--
0.2--
0.1--
I
0
I
3
I
6
I
9
I
12
I
15
Weeks after arrival
p-valuesbetween consecutivesamplingswithingroup
Fig. 1. Mean OD-values demonstrating antibodies to Sarcoptes scabiei in sera repeatedly collected from 40 pigs in each of two herds using all in--all out production systems throughout the fattening period. In herd A (open squares), the pigs were treated with acaricides once upon arrival. In herd B (filled circles), no precautions to prevent sarcoptic mange were taken. Six pigs in herd A (all seronegative week 12) and one pig in herd B (seropositive week 12) were slaughtered before week 15 having reached market weight. * * * = p < 0.001; * * := p < 0.01 ; * = p < 0.05; p-values below 0.1 are given with figures.
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2.3. S t a t i s t i c s
Statistical c a l c u l a t i o n s c o n c e r n i n g a b s o r b a n c e v a l u e s b e t w e e n c o n s e c u t i v e s a m p l i n g o c c a s i o n s w i t h i n h e r d s w e r e m a d e as p a i r e d S t u d e n t ' s t-tests, w h i l e M a n n W h i t n e y U tests w e r e u s e d w h e n c o m p a r i n g the herds. W h e n c o m p a r i n g the p r e v a l e n c e o f s e r o p o s i -
On arrival
3 weeks after arrival
6 weeks after arrival
9 weeks after arrival
12 weeks after arrival
15 weeks after arrival
V"'l = investigated pen
~
= not investigated pen F ' ~ = dunging area
• = seropositive pig Fig. 2. No. of pigs with antibodies to S. scabiei through the fattening period in herd A. All pigs in the herd were treated with acaricides during the first week after arrival. In each investigated pen, sera from four randomly selected pigs were repeatedly collected throughout the fattening period (n = 40). Six of these pigs were slaughtered between week 12 and week 15 as they had reached market weight. None of them had previously expressed antibodies to S. scabiei.
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tive animals of the herds, chi-square tests ( X 2 tests) were used (this method was only used when the expected number of observations for all categories was at least five).
3. Results 3.1. Del~elopment o f antibodies to Sarcoptes scabiei in the fattening herds
All the designated pigs ( n = 4 0 per herd) were blood sampled on arrival and subsequently after 3, 6, 9 and 12 weeks. Only 34 animals in herd A and 39 animals in herd B were blood sampled on the last occasion, i.e., 15 weeks after arrival, due to slaughter of the remainder which had attained market weight. None of the six pigs slaughtered in herd A had expressed detectable levels of antibodies to S. scabiei during the fattening period, while the slaughtered pig of herd B showed serum antibodies to S. scabiei 12 weeks after arrival. On arrival at the fattening herds, the mean optical density (OD-value) of antibodies to S. scabiei was 0.082 _ 0.052 and 0.072 + 0.035 for herd A and B, respectively (Fig. 1). During the second half of the rearing period, the mean OD-value increased significantly (Herd A; p < 0.05-0.01, Herd B; p < 0 . 0 1 - 0 . 0 0 1 ) between the sampling occasions in both herds. This increase was more pronounced in the herd where no acaricidal treatment was performed. Despite the difference in mean OD-values between the herds during the late fattening period, no significant differences were found ( p = 0.068 at week 12 and p = 0.060 at week 15). The numbers and locations of the pigs with antibodies to S. scabiei are shown in Fig. 2 and Fig. 3. When applying the cut-off value 0.175, only a few pigs were seropositive on arrival. Twelve weeks after arrival, there were significantly ( p < 0.05) more seroposWeeks after arrival On arrival
3
6
9
12
15
I---1 = investigated pen lY"/21= not investigated pen [':7:1 = dunging area • = seropositive pig o = pig seropositive week 12, but slaughtered week 15 Fig, 3. Occurence of pigs with antibodies to S. scabiei throughout the fattening period in herd B. No precautions to prevent sarcoptic mange was perti~rmed in the herd. In each investigated pen, sera from four randomly selected pigs were repeatedly collected throughout the fattening period (n = 40). One pig, reached market weight and was slaughtered between week 12 and week 15. This pig expressed antibodies to S. scabiei 12 weeks after arrival.
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Table 1 Prevalence of animals seropositive to S. scabiei through the rearing period in two fattening herds with age segregated rearing systems. Precautions aimed at preventing sarcoptic mange were taken upon arrival in herd A, but not in herd B. Six pigs in herd A (all seronegative week 12) and one pig in herd B (seropositive week 12) were slaughtered before week 15 having reached market weight Week after arrival
0 3 6 9 12 15c 15~
Number of seropositive pigs
Prevalence (%) of seropositive pigs
Herd A
Herd B
X2-value
Herd A
Herd B
X2-value
3/40 5/40 3/40 6/40 8/40 11/34 11/40
1/40 2/40 4/40 12/40 16/40 17/39 18/40
ND ND ND 2.58 3.81 ~ 0.98 2.65
7.5 12.5 7.5 15.0 20.0 32.4 27.5
2.5 5.0 10.0 30.0 40.0 43.6 45.0
2.63 3.52 0.39 6.45 a 8. l0 b 2.66 6.62 b
aX2 >__3.8; p < 0.05. b)(2 >6.6; p < 0,01. = results obtained week 15. d = results obtained week 15. complemented with the results of week 12 for slaughtered pigs. ND = not calculated, expected number of observations less than 5.
itive pigs in herd B than in herd A (Table 1). As also seen in that table, a significantly higher proportion of seropositive animals was found in herd B from week 9 onwards when the X 2 calculations were based on the prevalence of seropositive pigs (i.e., correcting for n = 100 per herd). In Figs. 2 and 3 each pig seropositive to S. scabiei is represented by a dot. However, as these dots are correlated to the pen and not to the individual animal, the figures do not show the transient immune response to S. scabiei noticed in some individuals from both herds during the early fattening period. Therefore, the immune responses throughout the rearing period of the pigs seropositive to S. scabiei during the early fattening period are described below. On arrival, three pigs in herd A expressed antibodies to S. scabiei. The sera from two of these animals showed decreasing OD-values to S. scabiei on the two following sampling occasions and both pigs were seronegative to S. scabiei 6 weeks after arrival. From that time, the OD-values increased and both pigs were seropositive to S. scabiei from week 9 onwards. The third pig in herd A that was seropositive to S. scabiei on arrival remained so throughout the study. In herd B, one pig was seropositive on arrival. This animal showed decreasing OD-values during the early fattening period and was seronegative 9 weeks after arrival. On the following sampling occasions, the optical density increased and the animal was again seropositive to S. scabiei at 15 weeks after arrival. Three of the pigs which were seronegative to S. scabiei on arrival were seropositive three weeks later, two in herd A and one in herd B. One of these pigs in herd A was seronegative from the next sampling occasion onwards, while the other pig remained seropositive throughout the study. The pig from herd B was seronegative on the consecutive sampling occasion (week 6), but was again seropositive from week 9
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onwards. All pigs that showed detectable amounts of antibodies to S. scabiei from week 6 onwards remained seropositive throughout the rearing period.
4. Discussion
The development of antibodies to S. scabiei during the fattening period was studied in two herds purchasing fatteners and performing age segregated production systems. The incidence of animals seropositive to S. scabiei was initially low in both herds. A transient immune response to S. scabiei during the early fattening period, at arrival and 3 weeks later, was noticed in both herds. It appears very unlikely that the immunoglobulins specific to S. scabiei demonstrated in pigs at about 10-12 weeks of age should reflect maternal antibodies. Unless the piglets have been exposed to the mite, such antibodies have been shown to decline below detectable levels in the sera several weeks before that age, (N~ickler et al., 1992; Bornstein and Zakrisson, 1993). Further, the serum levels of immunoglobulins specific to S. scabiei have previously been shown to decline rather rapidly following acaricidal treatment of young pigs (Bomstein and Wallgren, 1996). Consequently, the declining levels of antibodies to S. scabiei found during the early part of the fattening period probably reflected the natural catabolism of antibodies following acaricidal treatment at the herd of origin close to trade (both herds) or at arrival at the fattening unit (treated herd). According to recommendations by the Swedish Animal Health Service, pigs sold as fatteners should be free from sarcoptic mange. Therefore, the transient serological responses to S. scabiei noticed in the two animals in herd B could possibly be explained by an acaricidal treatment prior to allocation. However, whether in fact pigs delivered to fattening enterprises have been treated or not with acaricides remains unknown and the presence of antibodies to S. scabiei found on arrival at the fattening units clearly indicate that animals sold as fatteners may be infected with S. scabiei. The spread of infections of S. scabiei was primarily seen in clusters located close to the pens with those pigs infected on arrival. This suggests a spread from pig to pig due to contact within pens and with adjacent pens, which is in accordance with the reported transmission of the infection between animals (Dobson and Davies, 1992). However, the possibility of a limited spread of the mites by fomites and phoresy (Arlian, 1989) could not be ruled out. Such a spread could possibly explain the sudden appearance of antibody positive pigs during the late fattening period in pens located far from the pens initially infected with the mites. However, it should be noted that the status of S. scabiei infections of the pigs in the pens from which no pigs were sampled (hatched pens in Figs. 2 and 3) was not known in the present study and therefore, could have been a source of infection. While the mean OD-value of antibodies to S. scabiei remained the same during the first six weeks of the rearing period in the treated herd, a statistically significant increase of the mean OD value was noticed as early as on the second sampling occasion in the non-treated herd. In addition, the increase in mean OD-values during the second half of the fattening period noticed in both herds was more pronounced in the non-treated herd. Thus, despite that six seronegative pigs in the treated herd were slaughtered due to
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reaching market weight before the last sampling occasion there was a higher mean OD-value seen in the non-treated herd at the two last sampling occasions. However, these distinctions were not statistically significant ( p < 0.07). Infections with S. scabiei were found to spread more rapidly in the non-treated herd, resulting in a significantly higher proportion of seropositive animals from week 9 onwards. Consequently, the acaricidal treatment on arrival at the fattening herd was concluded to decrease and to delay the spread of sarcoptic mange during the fattening period, as previously suggested by others (Hogg, 1984; Soil and Smith, 1987; Roppa et al., 1988; Primm et al., 1992; Hollanders et al., 1995) Contrary to Hogg (1984) but in accordance with Hiepe et al. (1989), a single injection with ivermectin was not found to be adequate to eradicate sarcoptic mange in the present study. This could have several explanations. To perform the control program, all pigs were to be injected subcutaneously on one occasion close to arrival. The dosage used was 10 mg ivermectin per pig, corresponding to the treatment dose for a pig at a weight of 33 kg. As the mean weight of pigs on arrival at fattening enterprises is around 22-25 kg, underdosing of the drug would therefore be excluded. Instead, the labour when injecting the pigs should be taken into account. Injecting a large number of pigs subcutaneously in less than a day is a hard and stressful experience for both people and pigs. Failure to correctly inject some pigs infected with S. scabiei therefore, appears to be the most plausible explanation for failure to eradicate the mite from the herd. It has been established that to achieve an efficient therapeutic result it is of paramount importance to avoid injecting the active substance in fatty tissue (Schultz et al., 1988). Therefore, the common strategy of treating animals at least twice in eradication programmes on herd level (Henriksen et al., 1987; Jensen et al., 1988; Madsen, 1990; Bornstein et al., 1994), mainly induced by fear of incorrect injection of some individuals, appears to be appropriate.
5. Conclusion
There was a low prevalence of pigs with antibodies to S. scabiei found among pigs at the weight of about 25 kg, i.e., when the fattening herds were established. These seropositive pigs appeared to spread the infection within the herds, which was primarily demonstrated during the second half of the rearing period. A single injection with iverrnectin on arrival decreased and delayed the spread of the infection but did not eradicate the disease. The results of the study clearly indicate that at present conventional pigs sold as fatteners should not be considered to be free from infections with S. scabiei and that precautions to prevent sarcoptic mange are therefore justifiable in fattening herds. However, the results obtained also indicate that some piglet producing herds appear to be free from infections with S. scabiei. Thus, if pigs from these herds could be isolated and not mixed with pigs from infected herds at the establishment of fattening groups, treatments with acaricides would not need to be performed in fattening herds which only receives pigs declared free from the disease. Methods of detecting antibodies to S.
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scabiei c o u l d b e v a l u a b l e m e a n s o f d i s c r i m i n a t i n g i n f e c t e d p i g l e t p r o d u c i n g h e r d s f r o m herds not infected.
Acknowledgements W e w i s h to t h a n k Dr. P e r B e s k o w a n d M r s . A. L i l b u r n f o r v a l u a b l e h e l p a n d M r s . B. Christensson for skilful technical assistance. This study was supported by grants from the National Veterinary Institute.
References Arends, J.J., Stanislaw, C.M., Gerdon, D., 1990. Sarcoptic mange on lactating swine and growing pigs. J. Anim. Sci. 68, 1495-1499. Arlian, L.G., 1989. Biology, host relations and epidemiology of Sarcoptes scabiei, Ann. Rev. Entomol. 34, 139-161. Bogatko, W., 1974. Studies on the occurrence of Sarcoptes scabiei var suis (Gerlach, 1857) in clinically normal animals. Medycyna wet. 30, 38-39, Summary in English. Bornstein, S., Wallgren, P., 1996. Serum antibody responses to Sarcoptes scabiei infections in young pigs following acaricidal treatment. Proc. 14th Int. Pig Vet. Soc. Congr., Bologna, Italy, p. 355. Bornstein, S., Wallgren, P., 1997. Serodiagnosis of sarcoptic mange in swine. Vet. Rec. 141, 8-12. Bornstein, S.. Zakrisson, G., 1993. Clinical picture and antibody response in pigs infected by Sarcoptes scabiei vat suis. Vet. Derm. 4, 123-131. Bornstein, S.. FellstriSm, C., Thebo, P., Wallgren, P., 1994. Eradication of sarcoptic mange in a herd of pigs monitored by skin scrapings and ELISA. Proc. 13th Int. Pig Vet. Soc. Congr., Bangkok, Thailand, p. 251. Dobson, K.J., Davies, P.R., 1992. External parasites. In: Leman, A.D., Straw, B.E., Mengeling, W.L., D'Allaire, S., Taylor, D.J. (Eds.), Diseases of swine. Wolfe Publishing. Ames, IA, pp. 668-679. Gaafar, S.M., Arends, J.J., Hogg, A., Holster, K.H., Williams. R.E., 1986. An integrated program using tactic to control mange in swine. J. Agri, Entomol. 3, 374-381. Guit~rrez, J.F., de Vigo, J,M., Castella', J., Munos, E., Ferrer, D.. 1996. Prevalence of sarcoptic mange in fattening pigs sacrificed in a slaughterhouse of northeastern Spain. Vet. Parasitol. 61, 145-149. Henriksen, S.A., Ebbesen, T.J., Nielsen, K.V., 1987. Eradication of mange from a large sow- and slaughter pig herd. Dansk Vet.tidskr. 70, 575-579, Summary in English. Hiepe, T., Matthes, H.F., Werner, G., Zophel. W., Stark, H., Engel, H.G., 1989. Use of ivermectin to eradicate clinical sarcoptic mange in an intensive pig breeding and fattening unit. Mh. Vet. Med. 44, 501-503. Hogg, A., 1984. Eradication of sarcoptic mange in swine with ivermectin. Proc. 8th Int. Pig Vet. Soc. Congr., Ghent, Belgium, p. 206. Hollanders, W., Harbers, A.H.M., Huige, J.C.M., Monster, P., Rambags, P.G.M., Hendrikx, W.M.L., 1995. Control of Sarcoptes scabiei var. suis with ivermectin: Influence on scratching behaviour of fattening pigs and occurrence of dermatitis at slaughter. Vet. Paras itol. 58, 117-127. Jensen, J.C.E., Havn, C.V., Lind, O., 1988. Combined eradication of mange and dysentery in a mayor sow and slaughter pig herd. Dansk Vet, Tidsskr. 71, 105-112, Summary in English. Madsen, S.A., 1990. Eradication of mange in pigs with Sebacil pour-on :': in combination with Ivomec '~ (ivermectin) and Sebacil linament c~' 50%, Proc. l lth Int. Pig Vet. Soc. Congr., Lausanne, Switzerland, p. 206. Ntickler, K., Matthes, H-F., Hiepe, T.H., Ziegler, H., 1992. Nachweis von Anti-Sarcoptes suis IgG im Blutserum neonatal mit Sarkoptesmilben infizierten Ferkel mit dem indirekten ELISA. Mh. Vet. Med. 47, pp. 415-421. Palmer, E., 1989. The prevalence of hepatic milk spots in pigs at slaughter can be reduced with ivermectin. Svensk Vet. tidn. 41, 853-855, Summary in English.
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Primm, N.D., Hall, W.F., Di Pietro, J.A., 1992. Efficacy of an in-feed preparation of ivermectin against endoparasites and scabies mites in swine. Am. J. Vet. Res. 53, 508-512. Roppa, L., Bordin, E.L., Rotta, A., Salvador, N., Guerro, J., 1988. Effects of ivermectin on weight gain and feed conversion of fattening pigs. Proc. 10th Int. Pig Vet. Soc. Congr., Rio de Janeiro, Brazil, p. 262. Schultz, K., B~ickstriSm, L., Schultz, R., 1988. Antibody response of pigs to antigens administered intramuscularly or in the subcutaneous fat. Proc. 10th Int. Pig Vet. Soc. Congr., Rio de Janeiro, Brazil, p. 27. Soll, M.D., Smith, C.J.Z., 1987. Efficacy of ivermectin against the pig mite Sarcoptes s~lbiei var suis. J.S. Afr. Vet. Assoc. 58, 29-30.
Veterinary Parasitology 73 (1997) 315-324
The spread of porcine sarcoptic mange during the fattening period revealed by development of antibodies to Sarcoptes scabiei Per Wallgren a,*, Set Bornstein b a Department of Ruminant and Porcine Diseases, National Veterinary Institute, Box 7073, 750 07 Uppsala, Sweden b Department of Parasitology, National Veterinary Institute, Box 7073, 750 07 Uppsala, Sweden
Received 12 February 1997; accepted 29 May 1997
Abstract Using an indirect ELISA based on a whole body homogenate of Sarcoptes scabiei var vulpes, the development of serum antibodies to S. scabiei var suis during the fattening period was studied in two herds, purchasing fatteners and performing age segregated production systems. All the pigs in one of the herds were treated with ivermectin on the same day within a week after arrival, while no precautions were made to prevent sarcoptic mange in the other herd. In both herds, a transient immune response to S. scabiei was detected in some animals during the early fattening period, reflecting that these pigs had been exposed to S. scabiei before delivery to the fattening units. It also indicated that they had been treated with acaricides close to allocation. The incidence of animals seropositive to S. scabiei was initially low in both herds. The infection spread gradually as indicated by increasing optical densities of antibodies to S. scabiei, especially during the second half of the rearing period. This increase was more pronounced in the herd which had received no prophylactic treatment to sarcoptic mange. The infection with S. scabiei was found to have spread to more animals towards the end of the fattening period in that herd. It was concluded that a single injection with the acaricide on arrival at the fattening farm decreased and delayed the spread of the infection, but did not eradicate the mite infection. The results showed that conventional pigs sold as fatteners at present may be infected with S. scabiei and that precautions aimed at preventing sarcoptic mange therefore, are indicated in fattening herds. In this context, the ELISA employed could be a valuable means of discriminating between S. scabiei var suis infected piglet producing herds and uninfected herds. © 1997 Elsevier Science B.V. Kew,ords: Pig-Arthropoda; Sarcoptes scabiei; Mange; Immune response-arthropoda; Fatteners; Epidemiology
* Corresponding author. Tel.: +46-18-674000; fax: +46-18-309162. 0304-4017/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PII S0304-4017(97)001 18-0
316
P. Wallgren, S. Bornstein / Veterina O' Parasitology 73 (1997) 315-,¢24
1. Introduction
One of the most economically significant parasitic diseases within modem pig production is sarcoptic mange, caused by the itch mite Sarcoptes scabiei vat suis (Dobson and Davies, 1992). S. scabiei infections cause the swine industry substantial economic losses. According to previously published reports, an infected sow in USA will cost 84-115 US dollars annually due to decreased productivity (Gaafar et al., 1986; Arends et al., 1990). The prevalence of sarcoptic mange is reported to vary from 20 to over 90% within swine populations and 70 to 90% of the herds are reported to be infected with S. scabiei (Dobson and Davies, 1992; Guit~rrez et al., 1996). Although there are effective acaricides available and although these drugs are used in large quantities both prophylactically and therapeutically, high prevalence of S. scabiei infection is still common. The generally recommended and often employed management practice of prophylactically treating herds for sarcoptic mange, (e.g., acaricidal treatment of sows 1-4 weeks prior to farrowing or treatment on herd basis once every 6-12 months), does not eradicate S. scabiei from swine herds. Instead, such programmes often reduce the degree of infection in the herds to subclinical rates. Thus, the infection is maintained on a herd basis and some animals remain as carriers of the mites (Bogatko, 1974). Pig fattening enterprises, which buy pigs at 22-25 kg body weight from several different piglet producers are continuously confronted with the risk of introducing S. scabiei infections into their herds. In this context it should be clarified that the all in-all out production system in itself does not give protection against the disease since these herds are repeatedly restocked through purchase of pigs of unknown status regarding S. scabiei (as well as other infections). Therefore, several farm managers have applied acaricidal treatment to all their animals at the time of restocking in order to prevent the development of sarcoptic mange (Palm6r, 1989). The aim of this work was to study whether infections with S. scabiei occur in specialised fattening herds employing age segregated rearing systems. For this purpose S. scabiei antibody detection by an indirect ELISA was employed in two herds throughout the fattening period. In one of the herds, precautions aimed at combating sarcoptic mange were performed, while no such efforts were made in the other herd.
2. Materials and methods 2.1. Herds and experimental design
Two specialised fattening herds, rearing pigs from 25 to 107 kg live body weight, were chosen for the study. Both herds consisted of a single unit and applied the all in-all out production system. Herd A housed 485 pigs in 62 pens located in lbur rows and herd B housed 220 pigs in 22 pens located in two rows. In both herds, straw was provided daily. The lying area of the pens had solid floors, while the dunging areas
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consisted of slatted floors. Nose to nose contacts with pigs in adjacent pens in the same row as well as with pigs in facing pens on the opposite side of the dunging area were possible through the fences of the pens. To prevent sarcoptic mange, all pigs in herd A were injected subcutaneously with l0 mg ivermectin (Ivomec, MSD, Rahway, U S A ) during the first week after arrival at the herd. In herd B, no precautions against sarcoptic mange were taken. In both herds, four pigs from each of the 10 pens were randomly chosen for the study. These pigs were repeatedly blood sampled by jugular vein punctures using evacuated glass tubes without additives (Becton Dickinsson, Meylan Cedes, France) every third week during the rearing period (i.e., during week 0, 3, 6, 9, 12 and 15). The pens housing the sampled pigs were evenly distributed within the fattening units.
2.2. Detection o f antibodies to Sarcoptes scabiei
Antibodies to S. scabiei were estimated by an indirect E L I S A earlier described (Bornstein and Zakrisson, 1993; Bornstein and Wallgren, 1997). In brief, duplicates of sera diluted 1 / 2 0 0 were analyzed in microtiter plates (Greiner labortechnik, Frickenhausen, Germany) coated with a whole body homogenate of S. scabiei var vulpes diluted in 0.1 M carbonate buffer (pH 9.6). On each microtiter plate, positive and negative controls were employed and the optical density of each plate was corrected to a value of A492 = 1.05 for the positive control sera. The cut-off value lbr samples tested was previously defined as A492 >_ 0.175, corresponding to the mean value plus 3 S.D. of SPF sows (Bornstein and Wallgren, 1997).
density
0.3--
0.2--
0.1--
I
0
I
3
I
6
I
9
I
12
I
15
Weeks after arrival
p-valuesbetween consecutivesamplingswithingroup
Fig. 1. Mean OD-values demonstrating antibodies to Sarcoptes scabiei in sera repeatedly collected from 40 pigs in each of two herds using all in--all out production systems throughout the fattening period. In herd A (open squares), the pigs were treated with acaricides once upon arrival. In herd B (filled circles), no precautions to prevent sarcoptic mange were taken. Six pigs in herd A (all seronegative week 12) and one pig in herd B (seropositive week 12) were slaughtered before week 15 having reached market weight. * * * = p < 0.001; * * := p < 0.01 ; * = p < 0.05; p-values below 0.1 are given with figures.
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2.3. S t a t i s t i c s
Statistical c a l c u l a t i o n s c o n c e r n i n g a b s o r b a n c e v a l u e s b e t w e e n c o n s e c u t i v e s a m p l i n g o c c a s i o n s w i t h i n h e r d s w e r e m a d e as p a i r e d S t u d e n t ' s t-tests, w h i l e M a n n W h i t n e y U tests w e r e u s e d w h e n c o m p a r i n g the herds. W h e n c o m p a r i n g the p r e v a l e n c e o f s e r o p o s i -
On arrival
3 weeks after arrival
6 weeks after arrival
9 weeks after arrival
12 weeks after arrival
15 weeks after arrival
V"'l = investigated pen
~
= not investigated pen F ' ~ = dunging area
• = seropositive pig Fig. 2. No. of pigs with antibodies to S. scabiei through the fattening period in herd A. All pigs in the herd were treated with acaricides during the first week after arrival. In each investigated pen, sera from four randomly selected pigs were repeatedly collected throughout the fattening period (n = 40). Six of these pigs were slaughtered between week 12 and week 15 as they had reached market weight. None of them had previously expressed antibodies to S. scabiei.
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tive animals of the herds, chi-square tests ( X 2 tests) were used (this method was only used when the expected number of observations for all categories was at least five).
3. Results 3.1. Del~elopment o f antibodies to Sarcoptes scabiei in the fattening herds
All the designated pigs ( n = 4 0 per herd) were blood sampled on arrival and subsequently after 3, 6, 9 and 12 weeks. Only 34 animals in herd A and 39 animals in herd B were blood sampled on the last occasion, i.e., 15 weeks after arrival, due to slaughter of the remainder which had attained market weight. None of the six pigs slaughtered in herd A had expressed detectable levels of antibodies to S. scabiei during the fattening period, while the slaughtered pig of herd B showed serum antibodies to S. scabiei 12 weeks after arrival. On arrival at the fattening herds, the mean optical density (OD-value) of antibodies to S. scabiei was 0.082 _ 0.052 and 0.072 + 0.035 for herd A and B, respectively (Fig. 1). During the second half of the rearing period, the mean OD-value increased significantly (Herd A; p < 0.05-0.01, Herd B; p < 0 . 0 1 - 0 . 0 0 1 ) between the sampling occasions in both herds. This increase was more pronounced in the herd where no acaricidal treatment was performed. Despite the difference in mean OD-values between the herds during the late fattening period, no significant differences were found ( p = 0.068 at week 12 and p = 0.060 at week 15). The numbers and locations of the pigs with antibodies to S. scabiei are shown in Fig. 2 and Fig. 3. When applying the cut-off value 0.175, only a few pigs were seropositive on arrival. Twelve weeks after arrival, there were significantly ( p < 0.05) more seroposWeeks after arrival On arrival
3
6
9
12
15
I---1 = investigated pen lY"/21= not investigated pen [':7:1 = dunging area • = seropositive pig o = pig seropositive week 12, but slaughtered week 15 Fig, 3. Occurence of pigs with antibodies to S. scabiei throughout the fattening period in herd B. No precautions to prevent sarcoptic mange was perti~rmed in the herd. In each investigated pen, sera from four randomly selected pigs were repeatedly collected throughout the fattening period (n = 40). One pig, reached market weight and was slaughtered between week 12 and week 15. This pig expressed antibodies to S. scabiei 12 weeks after arrival.
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Table 1 Prevalence of animals seropositive to S. scabiei through the rearing period in two fattening herds with age segregated rearing systems. Precautions aimed at preventing sarcoptic mange were taken upon arrival in herd A, but not in herd B. Six pigs in herd A (all seronegative week 12) and one pig in herd B (seropositive week 12) were slaughtered before week 15 having reached market weight Week after arrival
0 3 6 9 12 15c 15~
Number of seropositive pigs
Prevalence (%) of seropositive pigs
Herd A
Herd B
X2-value
Herd A
Herd B
X2-value
3/40 5/40 3/40 6/40 8/40 11/34 11/40
1/40 2/40 4/40 12/40 16/40 17/39 18/40
ND ND ND 2.58 3.81 ~ 0.98 2.65
7.5 12.5 7.5 15.0 20.0 32.4 27.5
2.5 5.0 10.0 30.0 40.0 43.6 45.0
2.63 3.52 0.39 6.45 a 8. l0 b 2.66 6.62 b
aX2 >__3.8; p < 0.05. b)(2 >6.6; p < 0,01. = results obtained week 15. d = results obtained week 15. complemented with the results of week 12 for slaughtered pigs. ND = not calculated, expected number of observations less than 5.
itive pigs in herd B than in herd A (Table 1). As also seen in that table, a significantly higher proportion of seropositive animals was found in herd B from week 9 onwards when the X 2 calculations were based on the prevalence of seropositive pigs (i.e., correcting for n = 100 per herd). In Figs. 2 and 3 each pig seropositive to S. scabiei is represented by a dot. However, as these dots are correlated to the pen and not to the individual animal, the figures do not show the transient immune response to S. scabiei noticed in some individuals from both herds during the early fattening period. Therefore, the immune responses throughout the rearing period of the pigs seropositive to S. scabiei during the early fattening period are described below. On arrival, three pigs in herd A expressed antibodies to S. scabiei. The sera from two of these animals showed decreasing OD-values to S. scabiei on the two following sampling occasions and both pigs were seronegative to S. scabiei 6 weeks after arrival. From that time, the OD-values increased and both pigs were seropositive to S. scabiei from week 9 onwards. The third pig in herd A that was seropositive to S. scabiei on arrival remained so throughout the study. In herd B, one pig was seropositive on arrival. This animal showed decreasing OD-values during the early fattening period and was seronegative 9 weeks after arrival. On the following sampling occasions, the optical density increased and the animal was again seropositive to S. scabiei at 15 weeks after arrival. Three of the pigs which were seronegative to S. scabiei on arrival were seropositive three weeks later, two in herd A and one in herd B. One of these pigs in herd A was seronegative from the next sampling occasion onwards, while the other pig remained seropositive throughout the study. The pig from herd B was seronegative on the consecutive sampling occasion (week 6), but was again seropositive from week 9
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onwards. All pigs that showed detectable amounts of antibodies to S. scabiei from week 6 onwards remained seropositive throughout the rearing period.
4. Discussion
The development of antibodies to S. scabiei during the fattening period was studied in two herds purchasing fatteners and performing age segregated production systems. The incidence of animals seropositive to S. scabiei was initially low in both herds. A transient immune response to S. scabiei during the early fattening period, at arrival and 3 weeks later, was noticed in both herds. It appears very unlikely that the immunoglobulins specific to S. scabiei demonstrated in pigs at about 10-12 weeks of age should reflect maternal antibodies. Unless the piglets have been exposed to the mite, such antibodies have been shown to decline below detectable levels in the sera several weeks before that age, (N~ickler et al., 1992; Bornstein and Zakrisson, 1993). Further, the serum levels of immunoglobulins specific to S. scabiei have previously been shown to decline rather rapidly following acaricidal treatment of young pigs (Bomstein and Wallgren, 1996). Consequently, the declining levels of antibodies to S. scabiei found during the early part of the fattening period probably reflected the natural catabolism of antibodies following acaricidal treatment at the herd of origin close to trade (both herds) or at arrival at the fattening unit (treated herd). According to recommendations by the Swedish Animal Health Service, pigs sold as fatteners should be free from sarcoptic mange. Therefore, the transient serological responses to S. scabiei noticed in the two animals in herd B could possibly be explained by an acaricidal treatment prior to allocation. However, whether in fact pigs delivered to fattening enterprises have been treated or not with acaricides remains unknown and the presence of antibodies to S. scabiei found on arrival at the fattening units clearly indicate that animals sold as fatteners may be infected with S. scabiei. The spread of infections of S. scabiei was primarily seen in clusters located close to the pens with those pigs infected on arrival. This suggests a spread from pig to pig due to contact within pens and with adjacent pens, which is in accordance with the reported transmission of the infection between animals (Dobson and Davies, 1992). However, the possibility of a limited spread of the mites by fomites and phoresy (Arlian, 1989) could not be ruled out. Such a spread could possibly explain the sudden appearance of antibody positive pigs during the late fattening period in pens located far from the pens initially infected with the mites. However, it should be noted that the status of S. scabiei infections of the pigs in the pens from which no pigs were sampled (hatched pens in Figs. 2 and 3) was not known in the present study and therefore, could have been a source of infection. While the mean OD-value of antibodies to S. scabiei remained the same during the first six weeks of the rearing period in the treated herd, a statistically significant increase of the mean OD value was noticed as early as on the second sampling occasion in the non-treated herd. In addition, the increase in mean OD-values during the second half of the fattening period noticed in both herds was more pronounced in the non-treated herd. Thus, despite that six seronegative pigs in the treated herd were slaughtered due to
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reaching market weight before the last sampling occasion there was a higher mean OD-value seen in the non-treated herd at the two last sampling occasions. However, these distinctions were not statistically significant ( p < 0.07). Infections with S. scabiei were found to spread more rapidly in the non-treated herd, resulting in a significantly higher proportion of seropositive animals from week 9 onwards. Consequently, the acaricidal treatment on arrival at the fattening herd was concluded to decrease and to delay the spread of sarcoptic mange during the fattening period, as previously suggested by others (Hogg, 1984; Soil and Smith, 1987; Roppa et al., 1988; Primm et al., 1992; Hollanders et al., 1995) Contrary to Hogg (1984) but in accordance with Hiepe et al. (1989), a single injection with ivermectin was not found to be adequate to eradicate sarcoptic mange in the present study. This could have several explanations. To perform the control program, all pigs were to be injected subcutaneously on one occasion close to arrival. The dosage used was 10 mg ivermectin per pig, corresponding to the treatment dose for a pig at a weight of 33 kg. As the mean weight of pigs on arrival at fattening enterprises is around 22-25 kg, underdosing of the drug would therefore be excluded. Instead, the labour when injecting the pigs should be taken into account. Injecting a large number of pigs subcutaneously in less than a day is a hard and stressful experience for both people and pigs. Failure to correctly inject some pigs infected with S. scabiei therefore, appears to be the most plausible explanation for failure to eradicate the mite from the herd. It has been established that to achieve an efficient therapeutic result it is of paramount importance to avoid injecting the active substance in fatty tissue (Schultz et al., 1988). Therefore, the common strategy of treating animals at least twice in eradication programmes on herd level (Henriksen et al., 1987; Jensen et al., 1988; Madsen, 1990; Bornstein et al., 1994), mainly induced by fear of incorrect injection of some individuals, appears to be appropriate.
5. Conclusion
There was a low prevalence of pigs with antibodies to S. scabiei found among pigs at the weight of about 25 kg, i.e., when the fattening herds were established. These seropositive pigs appeared to spread the infection within the herds, which was primarily demonstrated during the second half of the rearing period. A single injection with iverrnectin on arrival decreased and delayed the spread of the infection but did not eradicate the disease. The results of the study clearly indicate that at present conventional pigs sold as fatteners should not be considered to be free from infections with S. scabiei and that precautions to prevent sarcoptic mange are therefore justifiable in fattening herds. However, the results obtained also indicate that some piglet producing herds appear to be free from infections with S. scabiei. Thus, if pigs from these herds could be isolated and not mixed with pigs from infected herds at the establishment of fattening groups, treatments with acaricides would not need to be performed in fattening herds which only receives pigs declared free from the disease. Methods of detecting antibodies to S.
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scabiei c o u l d b e v a l u a b l e m e a n s o f d i s c r i m i n a t i n g i n f e c t e d p i g l e t p r o d u c i n g h e r d s f r o m herds not infected.
Acknowledgements W e w i s h to t h a n k Dr. P e r B e s k o w a n d M r s . A. L i l b u r n f o r v a l u a b l e h e l p a n d M r s . B. Christensson for skilful technical assistance. This study was supported by grants from the National Veterinary Institute.
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