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Praca oryginalna Original paper

Lameness is a common production-disease syn-drome in intensive dairy production. The high in-cidence (54.6 new cases/100 cows) and prevalence (20.6 per cent) of lameness cause serious economic problems and welfare implications (4, 12). The most common causes of lameness in dairy cows include sole ulcers, white line lesions and digital dermatitis (11, 19). An important environmental component in foot lesion development for cows in early lactation is connected with physical stressors associated with housing (3). The association of stress and pain with lameness has an adverse effect on fertility in dairy cows (5, 11, 14, 15, 25). Lameness in cows during the early postpartum period has been associated with a higher incidence of ovarian cysts and a lower ovarian activ-ity, and consequently a lower likelihood of pregnancy and lower fertility than in the case of non-lame cows (1, 7, 13, 15, 18, 24). Hoof lesions in cows, such as sole ulcers or white line lesions, result in significant differences in calving to first service and calving to conception intervals when compared with healthy cows (14). Another study demonstrated that the time from calving to conception was significantly longer in lame cows with multiple lesions in comparison to healthy cows (10). Time from calving to conception is similar in cows classifield as non-lame, moderately

lame or lame. In cows with different degrees of lame-ness during the first 8 weeks of postpartum the calving to conception interval varied, but the difference are not significant (9). Mastitis and lameness occurring during lactation have significant effects on open days and the number of artificial inseminations per concep-tion (27). The probability of culling cows increases in those who have difficult births, when twins are born or have shorter days to first insemination, or longer days to conception (28).

The objective of the study was to compare calving to first service and calving to conception intervals as well as the first and overall conception rates between cows classified as non-lame, moderately lame, or lame during the first four months after calving.

Material and methods

Herd. Polish Holstein-Friesian dairy cows were kept on a farm located in the Wielkopolska region. The cows were housed in tie stalls with access to a pasture and a cow-yard throughout the year. The average milk production for ap-proximately 250 cows was approx. 8054 kg. For study purposes the data were collected between 2008 and 2009 from 24 primiparous and 57 multiparous cows, which calved from October 2008 to April 2009. In the summer period cows were fed as follows: pasture from 8:00 AM in the

Associations between different degrees of lameness

in early lactation and the fertility of dairy cows

JAN OLECHNOWICZ, JĘDRZEJ M. JAŚKOWSKI

Institute of Veterinary Medicine, Faculty of Breeding and Biology of Animals, Poznan University of Life Sciences, Wolynska 35, 60-637 Poznan, Poland

Received 05.12.2013 Accepted 24.05.2014

Olechnowicz J., Jaśkowski J. M.

Associations between different degrees of lameness in early lactation and the fertility of dairy cows Summary

The objective of this study was to compare calving to first service and calving to conception intervals, as well as first and overall conception rates between cows classified as non-lame, moderately lame, or lame during the first four months after calving. During this period cows were examined for lameness every two weeks, and they were scored fortnightly using a 5-point locomotion scoring system according to Sprecher et al. (27). The data were collected between 2008 and 2009 from 24 primiparous and 57 multiparous cows, which calved from October 2008 to April 2009. Cows clinically lame had a longer time to first service when compared with cows which were never lame, and with mildly lame cows, but this difference was not significant. Similarly, no differences were found in time to conception. The mean number of services per conception was lower in lame than in non-lame cows. No significant associations were found in this study between different degrees of lameness and fertility.

Keywords: cows, locomotion score, lameness, calving to first service interval, calving to conception interval, conception rate

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morning up to 1:00 PM in the afternoon, feeding with a total mix ration (15 kg of corncob silage, 8 kg of beet pulps – 24% dry matter, 6 kg of lucerne hay-silage, 5 kg of grass hay-silage/day/cow). Moreover, cows received 8 kg of fresh green lucerne fodder/day/cow. After calving the cows were additionally fed a concentrate (7 kg/ d/cow). Every day the tie stalls were changed with new bedding before the re-turn of the cows from pasture. The claws of clinically lame cows were disinfected by Bioval (Biovet Drawalew SA) and treated with an antibiotic spray. Hoof trimming in the herd was performed twice a year, in November and April.

Locomotion scores. During the first 120 d postpartum the cows were examined for lameness every two weeks and they were scored fortnightly using a 5-point locomotion scoring system according to

Sprecher et al. (26). The cows were observed and scored by the same observer when they were standing or walking at a distance of 5 to 10 m in a cow-yard in the autumn and winter months, and on the pasture in the spring and summer months. At every evaluation the cows were classified into one of five categories of lameness: 1 – non-lame (normal gait), 2 – mildly lame, 3 – moderately lame, 4 – lame, and 5 – severely lame. Cows which scored ≥ 3 points were clas-sified as clinically lame (CL). The first group comprised these cows which were never lame during the first 120 d postpartum (n = 19), cows with 1 or 2 point scores in this period were classified into the second group (n = 20), while cows with at least 3 or 4 points and more were divided according to the cumulative locomotion scores, with the third group containing clinically lame cows with medium (11 to 14) cumulative locomotion scores, and the fourth group composed of cows clinically lame with high (15 to 29) cumulative locomotion scores.

Data collection. The following data were collected from the farm records for each cow: parity (1, 2, ≥ 3), calving date, first service date, dates of the following services, conception date, days from calving to first service, days from calving to conception, and number of services per conception. On this basis first service conception rates (%), overall conception rates (%), and percentages of pregnant cows in 100 and 200 days were calculated on this basis for each group.

Statistical analysis. Data (time to first service, time to conception, and services per conception) were analysed us-ing the Statistica statistical package (Version 8). Statistical analysis of the results was conducted using the two-way analysis of variance (ANOVA). The main factors considered in the analysis of variance included parity (1, 2, ≥ 3), and the group of cows (1, 2, 3 and 4). Significant differences between means were evaluated using the least significant difference test at P < 0.05 and P < 0.01. Data traits expressed in percent (first service conception rate, overall conception rate, and cows pregnant in 100 and 200 days) were tested by the Kruskal-Wallis nonparametric test (statistical pack-age, Version 8).

Results and discussion

Incidence of clinical lameness. The incidence of clinically lame cows in the successive weeks of early lactation is given in Fig. 1. The percentage of clinically lame cows increased in the successive weeks, except for the 8th week, in which it amounted to 12.4%. The

largest percentage of clinically lame cows was ob-served between weeks 14 and 16 postpartum, but the average percentage of cows with clinical lameness was 16.8%. Of the 81 cows during the first 120 d postpar-tum, 50.6% (41 cows) were at least once scored at ≥ 3 points. Results reported by many authors showed that lameness occurs in early lactation (3, 5, 6, 9). A high proportion of cases of foot lameness (65%) is found in the first 100 days of lactation (5). Claw disorders cause approximately 90% of lameness cases in dairy cattle (19). The incidence of lameness in cows demonstrates a significant seasonal variation (4, 19, 23). The mean incidence of lameness in the winter was higher than in the summer, which was associated with the housing period (4, 19). Certain foot lesions, e.g. sole ulcers and interdigital hyperplasia, develop slowly in winter and there may be a seasonal “carry over,” resulting in lame-ness occurrence in the summer (19). The important causal factor of seasonality is probably connected with conditions created by cow-cooling systems, humidity and heat stress (23). According to those authors all evaluated lameness conditions were most common in the summer. Lameness in cows during the first 30-35 d postpartum was associated with a higher incidence of ovarian cysts, a lower likelihood of pregnancy, and lower fertility than those in non-lame cows (7, 13, 15). The incidence of clinical lameness in cows in the period of 8 weeks postpartum was higher than in this study, amounting to 60% (9). Similarly, a high propor-tion of cases of clinically lame cows (65%) occurred in the first 100 days of lactation (5). A percentage of Fig. 1. The distribution percentage of cows classfield as clinically lame (i.e. locomotion score of 3 or 4), and non-lame (i.e. locomotion score of 1 or 2) in early lactation 92,6 9,4 85,2 14,8 83,6 16,4 87,6 12,4 81,5 18,5 80,3 19,7 79 21 75,4 24,6 0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%

Weeks after calving

14 16 12 10 8 6 4 2

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lame cows comparable to that reported in this paper was found by Kiliç et al. (13). The number of lame cows during the first 60 d postpartum was 56 out of 308 animals (18.2%).

Lameness. Nineteen (23%), twenty (25%), twenty one (26%), and twenty one (26%) of the 81 cows were classi-fied as non-lame, mildly lame, clinically lame with medium cumulative locomotion scores or clinically lame with high cumulative locomotion scores, respectively (Table 1).

Time from calving to first ser-vice and to conception period, and services per conception. The median time to first service

increased in individual groups of cows, but the dif-ferences were not significant. However, significantly shorter intervals from calving to first service were re-corded for older cows. Time to conception was shorter in both groups of clinically lame cows as compared with healthy cows and mildly lame cows; however, this difference was not significant. Parity had no effect on time from calving to conception. For healthy cows and mildly lame cows a larger number of services per conception was recorded when compared with both groups of clinically lame cows. Significant differences in these traits were found only between cows which were never lame and clinically lame cows with a high cumulative locomotion score (p < 0.05). Primiparous cows had a significantly lower number of services per conception when compared with older cows (p < 0.01).

The number of days after calving to conception de-pends on many factors such as voluntary waiting period, insemination techniques, calving season, management system and herd size, production level and parity (21). According to those authors the high number of days open does not necessarily reflect poor fertility, which can be a result of management decisions. Clinically lame cows showed an average increase of seven days in terms of calving to first service interval and an average increase of 11 days in calving to conception interval (14). The increase of these intervals was particularly marked for cows in which sole or white line lesions occurred between 36 and 70 days after calving. For these cows time intervals from calving to first service and from calving to conception were longer by 17 and 30 days (P < 0.01 and P < 0.05), respectively, when compared to cows without lesions. Similarly, cows scored on the basis of visual locomotion scoring (VLS ≥ 3) had a median calving to conception interval of 149 d as compared with 119 d for cows that maintained VLS ≤ 2 (P < 0.001) (1). Sprecher et al. (26) reported that cows with VLS > 2 had longer periods of days

to first service and days from calving to conception. Time from calving to conception in cows classified as non-lame, moderately lame or lame during the first 8 weeks postpartum was similar, amounting to 144, 135 and 135 days, respectively (9). In the study by those authors cows were examined weekly for lame-ness and scored on the basis of a 6-point locomotion scoring system first described by Sprecher et al. (26) and later modified by Garbarino et al. (7). The average time from calving to conception in lame cows with different degrees of lameness, classified as lame with low (12 to 24), medium (25 to 26) or high (28 to 35) cumulative locomotion scores, was longer (156 days), amounting to 109, 142 and 156 days, respectively, but the differences were non-significant. In the present study the mean time from calving to first service was longer in clinically lame cows with medium and high cumulative locomotion scores when compared with cows which were never lame and mildly lame cows. However, the difference was non-significant, probably because of the considerable variation of means and standard deviations. The mean time from calving to conception was significantly longer in lame cows with multiple lesions as compared with healthy cows (10). Melendez et al. (15) found no differences in days to first service in lame and non-lame cows (98.8 vs. 94.8 d). Significant, although weak associations were found between lameness and days to first service, days to last service and calving interval, but not between return rate (25). Lame cows required more services per conception (2.14) when compared with non-lame cows (1.72), and those differences were significant (5). In our study we observed a lower number of services per conception in clinically lame cows with high cumulative locomo-tion scores, as compared with cows which were never lame (P < 0.05).

Parity and lameness had the biggest effect on the interval from calving to the commencement of luteal Tab. 1. Mean time to first service, mean time to conception (days), and mean number of services per conception in non-lame and lame cows during the postpartum period (120 days)

Factor No. of cows Time to first service (days) Time to conception (days) Services per conception

Group of cows* 81 NS NS ** 1 19 90.3 ± 37.4 187.8 ± 122.3 2.7 ± 1.5a 2 20 98.4 ± 43.4 179.6 ± 88.9 2.7 ± 1.2 3 21 103.0 ± 38.0 151.8 ± 71.4 2.1 ± 0.9 4 21 110.7 ± 46.8 160.8 ± 79.0 2.0 ± 0.9a Parity 81 ** NS *** 1 24 119.0 ± 43.3aA 164.3 ± 77.0 1.8 ± 0.8A 2 26 89.0 ± 38.0B 160.1 ± 93.8 2.6 ± 1.1B ≥ 3 31 97 ± 39.4b 181.3 ± 99.8 2.6 ± 1.3B Explanations:*1 – cows never lame, 2 – cows mildly lame, 3 – cows clinically lame with medium (11 to 14) cumulative locomotion scores, 4 – cows clinically lame with high (15 to 29) cumulative locomotion scores; Means with different superscript letters differ significantly at p ≤ 0.05 (a, b), p ≤ 0.01 (A, B); ** P < 0.05, *** P < 0.01

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activity, on the interval from calving to the first ovulatory oestrus, and on the proportion of luteal activity during the first 60 days after calving (8). An increased number of days open from approximately 90 to > 300 days in the previous parity doubled the risk of live culling and death around calving (22).

Relationship between

lame-ness and fertility. The data concerning the relationship between lameness and fertility of cows are presented in Table 2. The first service conception rate was similar in the third and fourth groups of cows (from 28.6 to 33.3%), while it was the lowest in mildly lame cows. This difference was not significant. Similarly, the dif-ferences in overall conception rate between the groups of cows were not significant, but a higher percentage was recorded in both groups of lame cows. The percent-age of pregnant cows within 200 days after calving was higher in all groups than the percentage of pregnant cows within 100 days after calving. The percentage of pregnant cows between all groups of cows in both periods varied, especially in 100 days after calving; however, the difference was insignificant.

Data reported by many authors showed that sole ulcers are the main cause of clinical lameness in cows, which is associated with a deterioration of reproductive performance (5, 11, 13, 15, 25). However, results of some studies indicate low associations of hoof lesions with production and fertility (6, 20). The conception rate tended to be lower during the 63-day period be-fore lameness, and the average conception rate during lactation, in which foot lameness occurred, was 31 per cent as compared with 40 per cent in the other lactations (14). The pregnancy rate to first service was significantly lower in lame cows as compared with healthy cows (45.9 vs. 56.3%), with more services per conception (2.14 vs. 1.72, respectively) and increased cull rates (10.1 vs. 4.9%, respectively) (5). Within mean fertility parameters of lame and non-lame cows, Kiliç et al. (13) found significant differences in the overall pregnancy rates, amounting to 83.9 and 93.4%, re-spectively. High-producing dairy cows showed a high incidence of abnormal ovarian cycles with a prolonged luteal phase and anovulation (24). Both are associated with a reduced reproductive performance in terms of such parameters as conception rates and pregnancy rates within 100 days after calving. Clinically lame cows during the first 70 days in milking were 25% less likely to become pregnant as compared with non-lame cows (2). Morris et al. (18) showed a synergistic effect of lameness and high somatic cell counts in the milk of cows, resulting in a reduced likelihood of ovulation. The high number of somatic cells in lame cows was associated with a lower intensity of estrus symptoms and a lower rate of fertility of cows (16,

17). The first service conception rate and the number of services per conception were similar for cows with different postpartal health histories within 60 days after calving (6). Digital dermatitis showed heritable variation among cows and was moderately associated with lifespan and production (20). The data collected in our study presenting characteristic fertility of lame and non-lame cows are generally lower than those reported by other authors.

In conclusion, clinically lame cows required a longer time to first service as compared with cows which were never lame, and with mildly lame cows, but these dif-ferences were insignificant. Similarly, no difdif-ferences were recorded in terms of time to conception. The mean number of services per conception was lower in lame than in non-lame cows. In this study no significant associations were found between different degrees of lameness and fertility.

References

1. Alawneh J. I., Laven R. A., Stevenson M. A.: The effect of lameness on the fertility of dairy cattle in a seasonally breeding pasture-based system. J. Dairy Sci. 2011, 94, 5487-5493.

2. Bicalho R. C., Vokey F., Erb H. N., Guard C. L.: Visual locomotion scoring in the first seventy days in milk: impact on pregnancy and survival. J. Dairy Sci. 2007, 90, 4586-4591.

3. Chaplin S. J., Ternet H. E., Offer J. E., Logue D. N., Knight C. H.: A com-parison of hoof lesions and behaviour in pregnant and early lactation heifers at housing. Vet. J. 2000, 159, 147-153.

4. Clarkson M. J., Downham D. Y., Faull W. B., Hughes J. W., Manson F. J.,

Merritt J. B., Murray R. D., Rusell W. B., Sutherst J. E., Ward W. R.: Incidence

and prevalence of lameness in dairy cattle. Vet. Rec. 1996, 138, 563-567. 5. Collik D. W., Ward W. R., Dobson H.: Associations between types of lameness

and fertility. Vet. Rec. 1989, 125, 103-106.

6. Dohoo I. R.: The effect of calving to first service interval on reproductive performance in normal cows and cows with postpartal disease. Can. Vet. J. 1983, 24, 343-346.

7. Garbarino E. J., Hernandez J. A., Shearer J. K., Risco C. A., Thatcher W. W.: Effect of lameness on ovarian activity in postpartum Holstein cows. J. Dairy Sci. 2004, 87, 4123-4131.

8. García-Ispierto I., López-Gatius F., Santolaria P., Yániz J. L., Nogareda C.,

López-Béjar M.: Factors affecting the fertility of high producing dairy herds

in northeastern Spain. Theriogenology 2007, 67, 632-638.

9. Hernandez J. A., Garbarino E. J., Shearer J. K., Risco C. A., Thatcher W. W.: Comparison of the calving-to-conception interval in dairy cows with different degrees of lameness during the prebreeding postpartum period. J. Am. Vet. Med. Assoc. 2005, 227, 1284-1291.

10. Hernandez J. A., Shearer J. K., Webb D. W.: Effect of lameness on the calving- -to-conception interval in dairy cows. J. Am. Vet. Med. Assoc. 2001, 218, 1611-1614.

11. Hultgren J., Manske T., Bergsten C.: Associations of sole ulcer at claw trim-ming with reproductive performance, udder health, milk yield, and culling in Swedish dairy cattle. Prev. Vet. Med. 2004, 62, 233-251.

12. Huxley J. N.: Impact of lameness and claw lesions in cows on health and production. Livest. Sci. 2013, 156, 64-70.

13. Kiliç N., Ceylan A., Serin İ., Gökbulut C.: Possible interaction between lame-ness, fertility, some minerals, and vitamin E in dairy cows. Bull. Vet. Inst. Pulawy 2007, 51, 425-429.

Tab. 2. The relationship between traits of cows classified as non-lame, mildly lame and clinically lame and their fertility

Group

of cows No. of cows

First service conception rate (%) Overall conception rate (%) Cows pregnant 100 days after calving

(%)

Cows pregnant 200 days after calving

(%) 1 19 31.6 48.9 31.6 63.1 2 21 15.0 53.2 14.3 71.4 3 21 28.6 65.7 23.8 76.2 4 20 33.3 68.4 40.0 75.0 Explanation: as in Tab. 1.

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14. Lucey S., Rowlands G. J., Russell A. M.: The associations between lameness and fertility in dairy cows. Vet. Rec. 1986, 118, 628-631.

15. Melendez P., Bartolome J., Archbald L. F., Donovan A.: The association between lameness, ovarian cysts and fertility in lactating dairy cows. Theriogenology 2003, 59, 927-937.

16. Morris M. J., Kaneko K., Uppal S. K., Walker S. L., Jones D. N., Routly J. E.,

Smith R. F., Dobson H.: Effects of high somatic cell counts in milk on

repro-ductive hormones and oestrus behaviour in dairy cows with special reference to those with concurrent lameness. Anim. Reprod. Sci. 2013, 141, 20-25. 17. Morris M. J., Kaneko K., Walker S. L., Jones D. N., Routly J. E., Smith R. F.,

Dobson H.: Influence of lameness on follicular growth, ovulation, reproductive

hormone concentrations and estrus behavior in dairy cows. Theriogenology 2011, 76, 658-668.

18. Morris M. J., Walker S. L., Jones D. N., Routly J. E., Smith R. F., Dobson S. H.: Influence of somatic cell count, body condition and lameness on follicular growth and ovulation in dairy cows. Theriogenology 2009, 71, 801-806. 19. Murray R. D., Downham D. Y., Clarkson M. J., Faull W. B., Hughes

J. W., Manson F. J., Meritt J. B., Russel W. B., Sutherst J. E., Ward W. R.:

Epidemiology of lameness in dairy cattle: description and analysis of foot lesions. Vet. Rec. 1996, 138, 586-591.

20. Onyiro O. M., Andrews L. J., Brotherstone S.: Genetic parameters for digital dermatitis and correlations with locomotion, production, fertility traits, and longevity in Holstein-Friesian dairy cows. J. Dairy Sci. 2008, 91, 4037-4046. 21. Oseni S., Misztal I., Tsuruta S., Rekaya R.: Seasonality of days open in US

Holsteins. J. Dairy Sci. 2003, 86, 3718-3725.

22. Pinedo P. J., De Vries A.: Effect of days to conception in the previous lactation on the risk of death and live culling around calving. J. Dairy Sci. 2010, 93, 968-977.

23. Sanders A. H., Shearer J. K., De Vries A.: Seasonal incidence of lameness and risk factors associated with thin soles, white line disease, ulcers, and sole punctures in dairy cattle. J. Dairy Sci. 2009, 92, 3165-3174.

24. Shrestha H. K., Nakao T., Suzuki T., Higaki T., Akita M.: 2004: Effects of abnormal ovarian cycles during pre-service period postpartum on subsequent reproductive performance of high-producing Holstein cows. Theriogenology 2004, 61, 1559-1571.

25. Sogstad Å. M., Østerås O., Fjeldaas T.: Bovine claw and limb disorders related to reproductive performance and production diseases. J. Dairy Sci. 2006, 89, 2519-2528.

26. Sprecher D. J., Hostetler D. E., Kaneene J. B.: A lameness scoring system that uses posture and gait to predict dairy cattle reproductive performance. Theriogenology 1997, 47, 1179-1187.

27. Vacek M., Stadnik L., Štipkova M.: Relationships between the incidence of health disorders and the reproduction traits of Holstein cows in the Czech Republic. Czech J. Anim. Sci. 2007, 52, 227-235.

28. Vries A. De, Olson J. D., Pinedo P. J.: Reproductive risk factors for culling and productive life in large dairy herds in the eastern United States between 2001 and 2006. J. Dairy Sci. 2010, 93, 613-623.

Corresponding author: Dr hab. Jan Olechnowicz, prof. nadzw., Osiedle Wichrowe Wzgórze 13/93, 61-675 Poznań; e-mail: olejanko@up.poznan.pl

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