One of the aims of organic production is to reduce the use of antibiotics in favour of using prophylactic measures as well as alternative therapies (Vaarst et al. Reference Vaarst, Bennedsgaard, Klaas, Nissen, Thamsborg and Ostergaard2006). Mastitis is one of the most important production problems in organic and conventional dairy herds and its therapy accounts for a very large proportion of the antibiotic drugs used in the farm. Somatic cell count (SCC), the main indicator of udder health status, has been compared in organic and conventional systems worldwide but antibiotic usage has not been extensively taking into consideration (Bennedsgaard et al. Reference Bennedsgaard, Klaas and Vaarst2010). There are no studies about how lack of antibiotic usage affects udder health status from organic dairy farms in Spain so the aims of this study were to (i) compare udder health (by using the SCC) of organic farms that do not use antibiotics with that of organic and conventional farms that use antibiotic treatments and (ii) evaluate the influence of not using antibiotics on udder health.
Material and methods
Data on which this paper was based were collected within a big project to evaluate the nutritional and sanitary situation of organic dairy cattle in Spain. All organic dairy farms (n = 13) enrolled in Dairy Control Record (DCR) and with willingness to participate in the study were selected and divided according to the antibiotic usage: organic farms not using antibiotics (O, n = 6) and organic farms using antibiotics (within the legally permitted number of treatments: OA, n = 7). Conventional farms were selected in the neighbourhood of the organics on the basis of being grazing farms with similar management practices (CA, n = 5). Production and management summaries of the farm groups are presented in Table 1. Detailed data for individual farms is in online Supplementary Table S1.
Table 1. Summarised details of farms enrolled in this study: Organic farms without antibiotic treatments (O) and organic farms (OA) and conventional farms (CA) using antibiotic treatments. Data are presented as arithmetic mean (herd size, no of parturitions, milk yield, calving interval) and median (no of treatments/cow/year) and range
* OH 4 farms with breed diversity (36 crosses and 8 Brown Swiss). OA: 5 farms with breed diversity (26 crosses, 20 Brown Swiss)
† pre-dipping and post-dipping
‡ mean: 31% cows (range: 12–33%)
For each farm, SCC (obtained from monthly DCR) was evaluated in all lactating cows during the last complete lactation finished before April 2013 (O, n = 154; OA, n = 159; CA, n = 80). According to Reneau (Reference Reneau1986), monthly SCC was transformed in Linear Score (LS) from 1 to 9; LS < 4 was considered as an indicator of healthy udder, from 4 to 6 udders with subclinical mastitis and >6 clinical mastitis.
Statistical analyses were done using SPSS for Windows (V.20.0). SCC was transformed to base-10 logarithmic scale before statistical analysis. Because cows were from different herds, independent and identically distributed observations could not be assumed, so analyses were carried out with mixed models, in which variable ‘herd’ was introduced as a random factor. Type of farm (O, OA and CA) and parity number (primiparous heifers, 2nd–3rd parities and ≥4th parities) were introduced as fixed factors to check the effect on SCC and LS thresholds. To state production effect on SCC, individual milk yield was introduced in the analysis as a covariate. Bonferroni post-hoc analyses were performed. The effect of lactation stage on SCC was evaluated by using a repeated-measured ANOVA with type of farm and parity number as fixed main factors and sampling date (1–10 monthly controls) as repeated-measures effect.
Results and discussion
Table 2 shows SCC in organic and conventional farms in our study. Overall, SCC significantly (P < 0·001) varied regarding type of farm and increased with lactation number. SCC was statistically significantly higher (F 2,3920 = 9·116; P < 0·001) in O (173780) compared to both organic and conventional farms using antibiotics (OA: 107152; CA: 93325). When SCC was compared in organic and conventional farms worldwide, consensus has not been found and only restricted comparisons can be made between studies because data are based on field observations. Even though Hamilton et al. (Reference Hamilton, Emanuelson, Forslund, Hansson and Ekman2006) indicated lower SCC in organic dairy farms, other studies found the opposite to be true (Roesch et al. Reference Roesch, Doherr, Scharen, Schallibaum and Blum2007; Rozzi et al. Reference Rozzi, Miglior and Hand2007) or very little difference between both production systems (Vaarst et al. Reference Vaarst, Bennedsgaard, Klaas, Nissen, Thamsborg and Ostergaard2006).
Table 2. Comparison of somatic cell count (SCC) and proportion of monthly samples with different linear scores between organic farms without antibiotic treatments (O), organic farms with antibiotic treatments (OA) and conventional farms (CA). Different superscript letters in the same row indicate statistically significantly differences between different types of farms whereas different superscript numbers in the same column indicate statistically significantly differences between number of parities
Differences between farms using and not using antibiotics increased with the number of parturitions. Considering primiparous heifers alone, significant differences were found between organic (O and OA, lower) and conventional farms (higher), whereas animals with more than 3 parities from group O showed statistically higher SCC than animals receiving antibiotics (OA and CA). Moreover, cows of group O showed higher increase of SCC with the number of parturitions (14·3%, calculated over log transformed data) compared to OA (7·1%) and CA (4·5%). It is well known that organic farms generally have older animals than conventional farms (Stiglbauer et al. Reference Stiglbauer, Cicconi-Hogan, Richert, Schukken, Ruegg and Gamroth2013) and lactation number have great influence in SCC (Reneau, Reference Reneau1986). In our study, organic farms had far more animals with more than 5 parities (O: 27·2%; OA: 24·8%) than conventional farms (3%). Taking into consideration that there are no differences in lactation number between both organic groups (O and OA), the differences on SCC found between organic farms using and not using antibiotics seem to indicate that sanitary measures to reduce SCC in O are less effective.
When evaluating the percentage of monthly milk samples with different LS thresholds for each complete lactation, it was observed that the percentage of healthy udders in group O was statistically lower (55·4%) compared to CA (77·5%), the group OA (68·0%) being between them. On the contrary, the percentage of LS indicating subclinical mastitis did not differ between group O (30·5%) and OA (25·4%), even though the percentage of clinical mastitis was statistically lower in group OA (6·61%) compared with group O (14·1%). Taking into consideration the number of parturitions, no differences between groups were observed for primiparous heifers. For the other parturition categories, the proportion of healthy udders (LS < 4) was significantly lower for group O, which, in addition, showed significantly higher incidence of subclinical mastitis (LS: 4–6) and clinical mastitis (LS > 6) in the older category. At the beginning of the productive cycle, organic cows not treated with antibiotics had similar or even better health status than the conventional ones. However, with increased parity, the proportion of O group cows with subclinical mastitis increased (and in the higher parities the proportion of those associated to clinical mastitis), presumably as a result of infection chronicity (Villar et al. Reference Villar, Gradillas, Fernández, Rodríguez-Bermúdez and López-Alonso2016). Older cows have greater risk of chronically higher SCC because of the accumulated risk of getting intrammamary infections that were not totally cured, resulting in a gradual increase in the number of infected quarters (Reneau, Reference Reneau1986) as well as in a decrease of curing rate after several antibiotic treatments (Swinkels et al. Reference Swinkels, Lam, Green and Bradley2013). The degree in which infection chronicity risk increases and cure rate decreases in herds not treated with antibiotics is not known and deserves more investigation.
Considering the production stage, SCC significantly varied throughout the lactation (F 9,414 = 26·138, P < 0·001) and all groups showed similar pattern, increasing from the 3rd month and recording their highest values towards the end of lactation (Fig. 1). There is a general consensus that SCC increases during lactation, whilst milk decreases due to a dilution effect, which explain, at least in part, the higher SCC found in organic farms compared to conventional ones, the latter having higher milk yields (Rozzi et al. Reference Rozzi, Miglior and Hand2007). In fact, milk production showed significant effect on SCC (F 1,4211 = 224·518; P < 0·001). However, Cicconi-Hogan et al. (Reference Cicconi-Hogan, Gamroth, Richert, Ruegg, Stiglbauer and Schukken2013) explain that the strength of this effect is low and deserves a more thorough investigation.
Fig. 1. Analysis of SCC in organic farms without antibiotic treatments (O), organic farms with antibiotic treatments (OA) and conventional farms (CA) considering the production stage by using a repeated-measured ANOVA.
In the scientific literature there is no agreement about how udder health should be monitored in organic farms. Antibiotic restrictions in the prophylaxis and treatment of udder infections (especially dry cow treatment) might be a cause of major problems of mastitis (Vaarst et al. Reference Vaarst, Bennedsgaard, Klaas, Nissen, Thamsborg and Ostergaard2006), but it does not seem to be convincingly demonstrated. Bennedsgaard et al. (Reference Bennedsgaard, Klaas and Vaarst2010) conclude that antibiotic udder treatments may be reduced without apparent negative effects and the control measures for SCC used on organic farms are at least as effective as those on conventional farms in controlling SCC. In this sense, preventive management practices are important in any dairy farm, but especially on organically managed farms, because the availability of products to treat disease is limited (Stiglbauer et al. Reference Stiglbauer, Cicconi-Hogan, Richert, Schukken, Ruegg and Gamroth2013).
In conclusion, SCC was higher in organic farms not using antibiotics compared with organic and conventional farms using antibiotic treatments. Udder health did not differ between organic and conventional farms for primiparous cows, but worsens throughout their productive life in the organics, possibly due to chronic infections related to limited use of antibiotics, showing higher occurrence of both subclinical and clinical mastitis in animals with 4 or more parities in farms not using antibiotic treatments. Although the reduction of antibiotics is needed on organic farms, measures to reduce SCC (especially in older cows) are not as effective as conventional measures, so preventive management practices are essential for mastitis control.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0022029916000601.
This work was supported by the Spanish Government (project code AGL2010-21026). Inmaculada Orjales holds a FPU fellowship (Ref. FPU14/01473) from the Spanish Ministry of Education, Culture and Sports. The authors thank all farmers who participated in the study and the staff of regional dairy laboratories for analysing milk samples.
Conflict of interest statement
None.
