association of growth performance with atrophic rhinitis and

Acta Veterinaria Hungarica 53 (3), pp. 287–298 (2005)

ASSOCIATION OF GROWTH PERFORMANCE WITH ATROPHIC RHINITIS AND PNEUMONIA DETECTED AT SLAUGHTER IN A CONVENTIONAL PIG HERD IN HUNGARY T. DONKÓ1*, Melinda KOVÁCS1 and T. MAGYAR2 1

Department of Physiology and Animal Hygiene, Faculty of Animal Science, Kaposvár University, Kaposvár, Hungary; 2Veterinary Medical Research Institute, Hungarian Academy of Sciences, Budapest, Hungary (Received January 4, 2005; accepted April 18, 2005) The influence of atrophic rhinitis (AR) and pneumonia on growth performance was assessed in a conventional farrow-to-finish pig farm affected by both diseases. All tested pigs (n = 138) were individually weighed at birth, at weaning, at moving to the growing/finishing unit, and at slaughtering. The extent (grade) of turbinate atrophy and lung consolidation attributable to pneumonia was determined in each pig at slaughter. A negative correlation was found between birth weight and the prevalence of nasal lesions at slaughter, suggesting that pigs born with smaller weight may be more susceptible to AR. The growth performance of the pigs also showed a negative correlation with the degree of turbinate atrophy. In the nursery period, the average daily gain (ADG) of pigs with moderate/severe turbinate atrophy was 13.3% lower than that of animals with healthy snouts. In the finishing period, pigs with mild AR lesions had an ADG reduction of 6.2%, while pigs with severe AR lesions had a significant, 9.4% reduction in ADG as compared to the AR-free pigs. The extent of weight gain reduction over the whole life cycle was very similar (approximately 6%) in the pigs having either AR or pneumonia alone. In those pigs where both respiratory diseases were present, their effects seemed to be added up (11.5%); however, nasal lesion scores and percentage of lung consolidation did not show statistically apparent interactive effects on growth performance. Key words: Swine, atrophic rhinitis, pneumonia, weight gain

Atrophic rhinitis of swine (AR) is a widely prevalent infectious disease of pig populations, characterised by twisting or shortening of the nose as a result of underlying atrophy of the bony structures of the nasal cavity. Toxigenic strains of Bordetella bronchiseptica and Pasteurella multocida are associated with the aetiology of AR (de Jong, 1999). Colonisation of the nasal mucosa by the aetiological agents and the production of the characteristic lesions of AR seem to be *

Corresponding author: Tamás Donkó; E-mail: [email protected]; Fax: +36 (82) 320 175 0236-6290/$ 5.00 © 2005 Akadémiai Kiadó, Budapest

288

DONKÓ et al.

age dependent. B. bronchiseptica infection should take place during the first weeks of life to give rise to remarkable turbinate atrophy (de Jong and Akkermanns, 1986) while, under predisposing conditions, P. multocida may successfully produce turbinate atrophy even at the age of 12–16 weeks (de Jong, 1999). In a survey conducted in Hungary, Szabó and Antal (1971) found that nearly 60% of the pig herds were severely affected by AR. However, they did not examine economic losses caused by the disease. Conflicting reports were published in the literature about the effect of AR on production parameters such as growth performance, feed conversion rate and days required to reach slaughter weight. A number of studies have reported an association between AR and retarded growth rate in some herds (Nielsen, 1983; Furukawa et al., 1989; Barfod et al., 1990; Paisley et al., 1993), whereas other studies could not reveal any relationship between the disease and the weight gain of pigs (Bendixen, 1971; Straw et al., 1984; Bäckström et al., 1985; Love et al., 1985; Dumas et al., 1990; Scheidt et al., 1990). Wilson et al. (1986) detected the harmful effect of AR on the growth rate in some herds but not in others. Diemen et al. (1995) revealed reduced activity and feed consumption in AR-affected pigs. Magyar et al. (2002) noticed the harmful effect of AR on the weight gain in experimentally infected pigs but these data cannot be extrapolated to naturally affected pig populations. The question is further complicated by the contradictory reports on the relationship between AR and pneumonia. Switzer et al. (1981) hypothesised that AR predisposes pigs to pneumonia while others (Wilson et al., 1986; Straw et al., 1989; Scheidt et al., 1992) did not see any connection between the presences of the two pathological conditions. Éliás et al. (1989) concluded, without giving further details, that AR and pneumonia – together and one by one – may cause remarkable financial deficits to the pig industry. The objective of the present study was to assess the influence of AR on growth performance in a conventional pig farm in Hungary. Furthermore, the relationship between pneumonia and growth rate was also investigated. Materials and methods The study was performed in a conventional farrow-to-finish operation in Hungary. The farm had 320 sows and produced approximately 6000 pigs per year. Clinical observation and slaughter evaluation of a representative number of finishing pigs indicated the AR-positive status of the herd. Bacteriological screening of 25 four-week-old pigs confirmed the presence of B. bronchiseptica and toxigenic P. multocida infection on the farm. Data collected from 138 randomly selected feeder pigs were included in the study. The piglets were individually marked with ear tattoos and followed up from birth until slaughtering. Pig production was performed in three stages. The Acta Veterinaria Hungarica 53, 2005

EFFECT OF ATROPHIC RHINITIS AND PNEUMONIA ON GROWTH PERFORMANCE IN PIGS 289

piglets observed during the study had come from two adjacent farrowing units. Each farrowing unit accommodated 17 dams together with their offspring. Seventy-seven pigs were born from 16 sows in the first unit and 61 pigs were born from 13 sows in the second unit. The average number of observed piglets was 4.76 per litter (range: 1–10). Males were castrated during the first week of life. Piglets were weaned at the age of 31–35 days, and then reared in a nursery in groups of eight until the approximate age of 90 days. Finally, the pigs were moved to a growing/finishing building where 28 pigs were housed in each pen. The farrowing units and the nursery were operated in ‘all in – all out’ system while the growing/finishing unit had continuous pig flow. All pigs were individually weighed at birth, at weaning, at moving to the growing/finishing building, and at slaughtering. The date of birth, the sow’s parity number, litter size, gender, dates of illnesses and treatments were also recorded. At slaughter, the lean meat percentage as well as the snout and lung lesions were evaluated in each test pig. The nose was cut transversally at the level of the first upper premolar teeth. Each of the four scrolls of the ventral turbinate bones was scored according to the following criteria (turbinate atrophy score): 0, no lesion; 1, a small part of the turbinate bone (nearly half a scroll) is absent; 2, slight atrophy – more than half a scroll is absent; 3, moderate atrophy – the turbinate bone is straightened; 4, severe atrophy – total disappearance of the turbinate bone. Nasal septum deviation was scored on a scale of 0–2: 0, normal; 1, slight deviation; 2, severe deviation. Turbinate atrophy and nasal septum deviation scores were summed for each individual to a maximum value of 18 (nasal lesion score). For statistical analysis, three groups of ranges were formed: grade 1 = scores 0–4, healthy; grade 2 = scores 5–8, mild lesion; grade 3 = scores 9–18, remarkable (moderate and severe) lesion. Gross pathological lung lesions were scored as described by Straw et al. (1989) for monitoring respiratory diseases in swine herds. The extension of consolidated areas attributable to pneumonia was recorded on schematic diagrams of the lungs. The percentage of each lobe and the total percentage of the lungs affected by pneumonia were estimated from these diagrams. Again, for statistical analysis, three groups of ranges were formed: grade 1 = lesion 0–5%, grossly normal/hardly affected; grade 2 = lesion 6–39%, moderately affected; grade 3 = scores 40% or more, severely affected. To compare the effect of lung and nasal lesions together and separately, respectively, four groups were assembled: 1, no lung and no nasal lesions; 2, nasal lesions but no lung lesions; 3, lung lesions but no nasal lesions and 4, both lesions are present. The measured bodyweight data were normally distributed. Least square means of the body weights and the mean daily gains were computed by LSMEANS method. Analysis of variance was done using the MIXED model of SAS 8.2 statistical software (SAS Institute Inc., 2001). The complete model was Acta Veterinaria Hungarica 53, 2005

290

DONKÓ et al.

adopted as follows: yijkl= µ + si + tj + lk + nl, where µ = the mean of all observations, si = the effect of the sex, tj = the effect of the litter size, lk = the effect of the lung lesion, nl = the effect of the nasal lesion. In another model only the last two variables were modified in the assembled groups. Spearman’s correlation analysis and two-way contingency table analyses with chi2 test were performed for the nose and lung scores and frequencies using SPSS for Windows 10.0 (2001) statistical software. Results The effect of the examined parameters on growth performance is summarised in Tables 1 and 2. There was no significant difference between litters of gilts and sows for body weight at any measuring point. A few suckling piglets (n = 12) were treated with antibiotics against transient alimentary disorders. However, these individual applications of medicines had no detectable effect on the weight gain. Therefore, these parameters were excluded from further evaluation of the results. The liveweights of castrated male and female pigs showed no difference until the age of 90 days. On the other hand, the castrates were 7 kg heavier than the females at the age of 190 days, and they needed 5 days less to reach market weight. Furthermore, their lean meat percentage was significantly higher than that of the females (53.8% versus 52.8%). Average birth weights were higher in smaller litters. This difference became even more remarkable by the age of 28 days. Considering the recorded parameters, only the litter size had an effect on the growth performance in the suckling period: piglets in larger litters grew slower than piglets in smaller litters. Interestingly, this difference in weight gain disappeared during the post-weaning period and was never noticed again. The nasal lesion scores recorded at slaughter varied from 0 to 18. The three groups formed by the three grades contained 46 (grade 1), 53 (grade 2), and 39 (grade 3) pigs, respectively. Neither the number of parity nor the gender had a significant effect on the extent of nasal lesions. Pigs showing grade 3 nasal lesions at slaughtering had significantly lower mean birth weight than pigs with a healthy nose (grade 1). There was no relationship between AR and the mean weaning weights of the pigs. AR-affected pigs started to show smaller weights later from the beginning of the fattening period (90 days of age) when pigs with severe nasal lesions (AR grade 3) weighed more than 3 kg (10%) less than pigs with AR grades 1 and 2. Significant growth performance differences were detected among the AR grade groups at slaughtering: grade 2 pigs had 4.8 kg (4%) while grade 3 pigs had 10.8 kg (9.5%) lower mean weights than grade 1 pigs. A significant negative correlation was found between slaughter weights and the degree of nasal lesions (r = –0.379; P < 0.001). This was also reflected in the numActa Veterinaria Hungarica 53, 2005


ber of days needed to attain slaughter weights: this value was 189, 192 and 197 for grade 1, 2 and 3, respectively. The difference between grade 1 and grade 3 groups was significant (P < 0.05). Average daily gain (ADG) showed a negative correlation with the extent of nasal lesions from the nursery period onwards. In the nursery period, ADG associated with moderate/severe (grade 3) turbinate atrophy was 13.3% lower than ADG of pigs with healthy snouts. In the finishing period, pigs with mild AR lesions had an ADG reduction of 6.2% while pigs with grade 3 AR lesions had a significant 9.4% reduction as compared to the pigs free of turbinate atrophy. ADG from birth until slaughter was different among all AR groups: the grade 2 group grew 4.3% whereas the group with grade 3 lesions grew 9.6% slower than the grade 1 group. Estimates of total consolidated lung volume attributable to pneumonia varied from 0 to 100%. The three groups formed by the three grades contained 52 (grade 1), 55 (grade 2), and 31 (grade 3) pigs, respectively. In the same way as for nasal lesions, the end of the nursery period was the first time when the effect of pneumonia on liveweight became apparent: at that time pigs with severe (grade 3) lung lesions weighed more than 2 kg (6%) less on the average than pigs with no or low percentage of lung consolidation (grades 1 and 2). Significant growth performance differences were detected among the three pneumonia grade groups at slaughtering: grade 2 pigs had 3 kg (3%) while grade 3 pigs had 9 kg (9.6%) smaller mean weights than grade 1 pigs. At the same time, only grade 3 percentage of pneumonia led to a significant extension of the growth and fattening period by an estimated 8 days as compared to the other two groups. During the growing period (from 28 to 90 days of age), the group of pigs with a high percentage of pneumonia (grade 3) had significantly (13%) lower ADG than grade 2 pigs. Interestingly, the ADG of grade 1 pigs fell between the ADG values of the grade 2 and 3 groups, and did not differ significantly from either of them. In the finishing period (from 90 to 190 days of age) ADG showed a negative correlation with the extent of lung lesions in all groups. Pigs with grade 2 lesions had an ADG reduction of 5.5% while pigs with grade 3 lesions had a reduction of 11% as compared to grade 1 pigs. Only severe pneumonia resulted in a significant (9.7%) decrease of ADG calculated from birth until slaughter. The frequency of turbinate atrophy was higher in pigs having lung lesions and vice versa: prevalence of pneumonia was higher among pigs with nasal lesions (grades 2 and 3) than in AR-negative pigs (grade 1) (Table 3). The odds ratio calculated from the frequency of AR and pneumonia indicates a 3.8 times higher probability of the two pathological conditions occurring together than either one alone. There was a rather weak but significant correlation between the severity of lung and nasal lesions, respectively (r = 0.269, P < 0.01). Nevertheless, nasal lesion scores and the percentage of lung consolidation did not show statistically apparent interactive effects on growth performance. Acta Veterinaria Hungarica 53, 2005

Acta Veterinaria Hungarica 53, 2005

73 65 23 89 26 52 55 31 46 53 39

n

1.65a 1.59ab 1.48b

1.63a 1.55b 1.55b 1.56 1.61 1.55

1.61 1.54

LSM

Birth

LSM: Least Square Means; SE: Standard Error; significantly (P < 0.05)

Male Female Litter size: < 8 Litter size: 9–11 Litter size: > 12 Lung lesion: grade 1 Lung lesion: grade 2 Lung lesion: grade 3 Nasal lesion: grade 1 Nasal lesion: grade 2 Nasal lesion: grade 3

Variable

8.59a 8.11b 7.40c 7.89 8.07 8.14 7.99 8.10 8.01

7.94 8.13

LSM

0.23 0.23 0.32 0.21 0.28 0.25 0.25 0.27 0.26 0.25 0.27

SE

31.39a 32.60a 29.53b 32.17a 32.38a 28.98b

30.97 31.38 31.87 31.19 30.47

LSM

90 days

0.95 0.99 1.36 0.88 1.16 1.03 1.07 1.14 1.08 1.05 1.12

SE

1.51 1.65 2.46 1.29 2.32 1.81 1.73 2.16 1.93 1.80 2.06

112.01a 105.39b 108.91 109.49 107.71 113.36a 110.23b 102.51c 113.89a 109.11b 103.10c

SE

LSM

190 days

190.42a 190.37a 198.06b 189.21a 192.23b 197.41b

190.27a 195.63b 193.32 193.49 192.04

LSM

1.24 1.38 2.03 1.06 1.94 1.49 1.42 1.80 1.59 1.48 1.72

SE

Age at 110 kg liveweight (day)

Means with different superscripts within the same column and the groups of variables differ

a, b, c

0.05 0.06 0.08 0.05 0.07 0.06 0.06 0.07 0.06 0.06 0.06

SE

28 days

Liveweight corrected to the same age (kg)

Effect of different parameters on weight and on the number of days needed to reach the slaughter weight

Table 1

292 DONKÓ et al.

73 65 23 89 26 52 55 31 46 53 39

n

249.9a 232.6a 207.2b 224.9 231.2 233.7 228.4 232.2 229.2

226.6 233.3

8.0 8.4 11.6 7.5 9.9 8.8 9.1 9.7 9.2 9.0 9.5 379.1ab 395.6a 345.0b 389.9a 391.6a 338.2b

371.4 375.1 375.4 372.2 372.0

14.6 15.2 21.0 13.6 17.9 15.9 16.4 17.6 16.7 16.2 17.3

SE

LSM

SE

LSM

12.7 13.9 20.8 10.9 19.6 15.3 14.6 18.2 16.3 15.2 17.4

802.0a 731.9b 760.3 774.4 766.0 811.6a 767.0b 722.1c 808.9a 758.7b 733.1b

SE

LSM

from 90 to 190 days

Average daily gain (g) from 28 to 90 days

from birth to 28 days

588.2a 571.8a 531.1b 591.0a 565.9b 534.2c

581.1a 546.3b 564.8 567.8 558.5

LSM

7.9 8.7 12.9 6.8 12.2 9.5 9.1 11.4 10.1 9.5 10.8

SE

from birth to 190 days

LSM: Least Square Means; SE: Standard Error; a, b, cMeans with different superscripts within the same column and the groups of variables differ significantly (P < 0.05)

Male Female Litter size: < 8 Litter size: 9–11 Litter size: > 12 Lung lesion: grade 1 Lung lesion: grade 2 Lung lesion: grade 3 Nasal lesion: grade 1 Nasal lesion: grade 2 Nasal lesion: grade 3

Variable

Effect of different parameters on weight and on the number of days needed to reach the slaughter weight

Table 2



294

DONKÓ et al.

Table 3 Relationship between frequency of nasal lesions and pneumonia Nasal lesion grade (NLG) 1

2–3

1

n % within LLG % within NLG

27 51.9% 58.7%

25 48.1% 27.2%

2–3

N % within LLG % within NLG

19 22.1% 41.3%

67 77.9% 72.8%

Lung lesion grade (LLG)

chi2 = 12.97; degree of freedom (df) = 1; P < 0.001

Pigs with nasal but no lung lesions as well as those with lung but no nasal lesions had significantly lower weight at slaughter: 8 kg (6.7%) and 7.4 kg (6.2%), respectively. Pigs in the group with both lesions were 13.7 kg (11.5%) lighter than those free of both AR and lung lesions (Table 4). Table 4 Relationship between the slaughter weight and the nasal lesions and/or pneumonia Nasal lesion grade (NLG)

Weight at 190 days (kg)

1

2–3

1

LSM SE n

118.9a 2.50 19

110.9b 2.58 67

2–3

LSM SE LSM

111.5b 2.82 118.9a

105.2c 1.63 110.9b

Lung lesion grade (LLG)

LSM: Least Square Means; SE: Standard Error; nificantly (P < 0.05)

a, b, c

Means with different superscripts differ sig-

Discussion Piglets born to gilts are usually smaller and weaker (Spicer et al., 1986) and considered more susceptible to the development of severe turbinate atrophy (Madec and Kobisch, 1985) than piglets born to higher-parity females. Our findings did not support these observations, although the number of gilts was rather Acta Veterinaria Hungarica 53, 2005


small in our study. The case was different if the prevalence of AR was considered: 80% of the pigs born to gilts had nasal lesions of certain degree whereas only 55% of the pigs born to older sows were affected by the disease. This difference proved to be significant (chi2 = 4.22; df = 1; P < 0.05). The higher slaughter weights of castrated males can be explained by the higher feed consumption rate and better growth performance of males as compared to females (Latorre et al., 2003). On the other hand, superior lean meat percentage of females over males suggests a more pronounced fat production ratio in the males (Kolstad et al., 1996). None of the other parameters examined here had an influence on the percentage of lean meat. This is inconsistent with the results of Hoy et al. (1989), who reported less favourable meat quality ranking in 15% of AR-affected pigs at slaughter. Hoy et al. (1989) detected milder AR lesions among females, supposing a reduced resistance of males due to stress caused by castration. Sex did not seem to have influence on the extent of nasal lesions in our case, which is consistent with the conclusion reached by Jackson et al. (1982). The birth weight of the piglets showed a negative correlation with the prevalence and the degree of nasal lesions. Pigs having moderate/severe turbinate atrophy at slaughter were born with smaller weights than pigs without ARspecific lesions. This finding suggests that the smaller birth weight may render pigs more susceptible to be successfully infected by B. bronchiseptica and P. multocida and to develop the disease. AR-affected pigs were reported to be born with 150 g smaller weights than AR-free pigs (Hoy et al., 1989). This difference was 170 g in our case. Smaller newborn piglets may less effectively accommodate to the circumstances of the farrowing units, and might be more easily attacked by various diseases. Heavier piglets have better position in struggling for feed; they can take higher amount of colostrum, thus gaining a better immune status (Bollwahn, 1982). At the same time, no such relationship was revealed between pneumonia and birth weight. A possible explanation is that AR-associated pathogens should infect pigs at a very young age to cause disease, which is not the case with several lung pathogens. Therefore, weakness at that age may facilitate the development of AR. No impact of AR on weights was noticed until the nursery period. In the suckling age, weight performance is mostly determined by birth weight, milk production of the sow, and the size of the litter, i.e. the influence of the dam is dominating. The higher birth and weaning weights usually found in smaller litters support this view. Piglets infected by the AR pathogens from the dam are less likely to develop remarkable lesions during the suckling period, thus their weights are primarily influenced by maternal factors at this age. The most characteristic lesions of AR may develop in the post-weaning growing phase. It is in harmony with our findings that AR-associated weight gain reduction was manifested from the nursery period to reaching market weight. Acta Veterinaria Hungarica 53, 2005

296

DONKÓ et al.

The growth performance of the pigs showed clear negative correlation with the extent of turbinate atrophy expressed as nasal lesion scores. Even the slightly affected pigs showed reduced weight gain that was doubled in pigs with remarkable nasal lesions at slaughter. The length of the finishing period was extended accordingly: pigs with mild lesions needed 3 days more whereas severely affected pigs needed 8 days more to attain slaughter weight than the AR-free pigs. Considering the whole life cycle, the presence of turbinate atrophy might be associated with significant weight gain reduction that showed a positive correlation with the nasal lesion scores. At the same time, only high percentages of lung consolidation had the same effect. Low prevalence of pneumonia did not influence the growth performance. The length of the finishing period was biased similarly: even low nasal lesion scores were accompanied by significant extension of the finishing period, while minor lung lesion percentages had no such effect. Again, only severe cases of pneumonia could be associated with impaired growth performance. This is in accordance with the observation of Straw (1991) who also found that only severe pneumonia caused remarkable weight gain reduction. No significant interaction was found between the effects of nasal lesions and pneumonia in any of the cases when both respiratory diseases caused weight gain reduction. The extent of weight gain reduction over the whole life cycle was very similar (approximately 6%) in the groups having either AR or pneumonia alone. In the pigs where both respiratory diseases were present, their effects seemed to be simply added up (11.5%) without fortifying the effects of each other. In a similar survey, only nasal lesions could be associated with reduced weight performance (Klawitter et al., 1988). These findings suggest that these conditions may manifest their harmful effect via different mechanisms. In summary, the results of the present study support the view that AR is able to cause a reduction in the growth performance of pigs, thus resulting in economic losses to pig production. Acknowledgements This work was supported by the Hungarian Scientific Research Fund (OTKA), grant No. T034650.

References Bäckström, L., Hoefling, D. C., Morkoc, A. C. and Cowart, R. P. (1985): Effect of atrophic rhinitis on growth rate in Illinois swine herds. J. Am. Vet. Med. Assoc. 187, 712–715. Barfod, K., Sorensen, V. and Nielsen, J. P. (1990): Methods of evaluation of atrophic rhinitis. Proc. Int. Congr. Pig Vet. Soc., Lausanne, Switzerland. p. 70. Bendixen, H. C. (1971): Chronic dystrophic s. atrophic s. infectious rhinitis in pigs (in Danish). Nord. Vet. Med. 23, Suppl. I, p. 171. Acta Veterinaria Hungarica 53, 2005


Bollwahn, W. (1982): Constitutionally predisposed diseases and performance shortcomings of fattened swine (in German). Tierärztl. Prax. 10, 175–182. De Jong, M. F. (1999): Progressive and nonprogressive atrophic rhinitis. In: Straw, B. E. (ed.) Diseases of Swine. 8th edition. Iowa State University Press, Ames, Iowa. pp. 355–384. De Jong, M. F. and Akkermans, J. P. W. M. (1986): I. Atrophic rhinitis caused by Bordetella bronchiseptica and Pasteurella multocida and the meaning of a thermolabile toxin of P. multocida. Vet. Quart. 8, 204–214. Diemen, P. M. van, de Jong, M. F. and Reilingh Schrama, J. W. (1995): Effects of atrophic rhinitis induced by Pasteurella multocida toxin on heat production and activity of pigs kept under different climatic conditions. J. Anim. Sci. 73, 1658–1665. Dumas, G., Denicourt, M., D’Allaire, S., Bigras-Poulin, M. and Martineau, G. P. (1990): Atrophic rhinitis and growth rate: A potential confounding effect related to slaughter weight. Proc. Int. Congr. Pig Vet. Soc., Lausanne, Switzerland. p. 385. Éliás, B. (1989): Report on the observations on the epizooties of infectious atrophic rhinitis in Hungary (in Hungarian, with English abstract). Magyar Állatorvosok Lapja 44, 587–593. Furukawa, S., Takami, H., Mori, Y., Nomura, S., Konishi, Y. and Shiraiwa, K. (1989): Effect of respiratory diseases on body weight gain in fattening pigs. J. Jap. Vet. Med. Assoc. 42, 793–796. Hoy, S., Mehlhorn, G., Lieschke, B., Ballinger, U., Dorn, W. and Warnecke, H. W. (1989): Influence of selected endogenous factors on the frequency and distribution of atrophic rhinitis in pigs (in German). Tierzucht 43, 430–432. Jackson, G. H., Evans, D. G. and Allen, M. M. (1982): The prevalence of nasal turbinate atrophy in British centrally-tested pigs. Br. Vet. J. 138, 480–488. Klawitter, E., Hoy, S. and Mehlhorn, G. (1988): Influence of inflammatory respiratory lesions on the liveweight gain of selected young and fattening pigs (in German). Monatsh. Vet.-med. 43, 597–600. Kolstad, K., Jopson, N. B. and Vangen, O. (1996): Breed and sex differences in fat distribution and mobilization in growing pigs fed at maintenance. Livestock Prod. Sci. 47, 33–41. Latorre, M. A., Lazaro, R., Gracia, M. I., Nieto, M. and Mateos, G. G. (2003): Effect of sex and terminal sire genotype on performance, carcass characteristics, and meat quality of pigs slaughtered at 117 kg body weight. Meat Sci. 65, 1369–1377. Love, R. J., Wilson, M. R. and Tasler, G. (1985): Porcine atrophic rhinitis. Aus. Vet. J. 62, 377–378. Madec, F. and Kobisch, M. (1985): Piglet pointers to respiratory disease. Pig Int. 11, 24–26. Magyar, T., King, V. L. and Kovács, F. (2002): Evaluation of vaccines for atrophic rhinitis – a comparison of three challenge models. Vaccine 20, 1797–1802. Nielsen, N. C. (1983): Prevalence and economic significance of atrophic rhinitis. In: Pedersen, K. B. and Nielsen, N. C. (eds) Atrophic Rhinitis in Pigs. Commission of the European Communities, Luxembourg. pp. 35–42. Paisley, L. G., Vraa-Andersen, L., Dybkjaer, L., Moller, K., Christensen, G., Mousing, J. and Agger, J. F. (1993): An epidemiologic and economic study of respiratory diseases in two conventional Danish swine herds. I: Prevalence of respiratory lesions at slaughter and their effects on growth. Acta Vet. Scand. 34, 319–329. SAS Institute (2001): The SAS System for Windows. Release 8.02, SAS Institute Inc., Cary, NC, USA. Scheidt, A. B., Mayrose, V. B., Hill, M. A., Clark, L. K., Cline, T. R., Knox, K. E., Runnels, L. J., Frantz, S. and Einstein, M. E. (1990): Relationship of growth performance to pneumonia and atrophic rhinitis detected in pigs at slaughter. J. Am. Vet. Med. Assoc. 196, 881–884. Scheidt, A. B., Mayrose, V. B., Hill, M. A., Clark, L. K., Einstein, M. E., Frantz, S. F., Runnels, L. J. and Knox, K. E. (1992): Relationship to growth performance of pneumonia and atrophic rhinitis lesions detected in pigs at slaughter among four seasons. J. Am. Vet. Med. Assoc. 200, 1492–1496.


298

DONKÓ et al.

Spicer, E. M., Driesen, S. J., Fahy, V. A., Horton, B. J., Sims, L. D., Jones, R. T., Cutler, R. S. and Prime, R. W. (1986): Causes of preweaning mortality on a large intensive piggery. Aus. Vet. J. 63, 71–75. SPSS Inc. (1999): SPSS for Windows. Version 10. Straw, B. E. (1991): Performance measured in pigs with pneumonia and housed in different environments. J. Am. Vet. Med. Assoc. 198, 627–630. Straw, B. E., Leman, A. D. and Robinson, R. A. (1984): Pneumonia and atrophic rhinitis in pigs from a test station — a follow-up study. J. Am. Vet. Med. Assoc. 185, 1544–1546. Straw, B. E., Tuovinen, V. K. and Bigras-Poulin, M. (1989): Estimation of the cost of pneumonia in swine herds. J. Am. Vet. Med. Assoc. 195, 1702–1706. Switzer, W. P., Engen, R. L., Ghoghal, N. G. and Kunesh, J. P. (1981): Respiratory system. In: Leman, A. D., Glock, R. D., Mengeling, W. L., Penny, R. H. C., Scholl, E. and Straw, B. (eds) Diseases of Swine. 5th edition. Iowa State University Press, Ames, Iowa. pp. 138–148. Szabó, I. and Antal, A. (1971): Controlling the freedom from atrophic rhinitis of swine breeding stocks (in Hungarian, with English abstract). Magyar Állatorvosok Lapja 26, 429–437. Wilson, M. R., Takov, R., Friendship, R. M., Martin, S. W., McMillan, I., Hacker, R. R. and Swaminathan, S. (1986): Prevalence of respiratory diseases and their association with growth rate and space in randomly selected swine herds. Can. J. Vet. Res. 50, 209–216.
