Macrae Investigation and reduction in inhibitory substance (antibiotic) failures in a UK producer group: 2014 - 2017
Investigation and reduction in inhibitory substance (antibiotic) failures in a UK producer group: 2014 – 2017
Macrae AI, Russell G, Forrest J, Burrough E and Corbishley A
Dairy Herd Health and Productivity Service, Division of Veterinary Clinical Sciences, Royal (Dick) School of Veterinary Studies and the Roslin Institute, University of Edinburgh, EBVC, Easter Bush, Roslin, Midlothian, EH25 9RG
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Alastair Macrae BVM&S, PhD, CertSHP, DCHP, DipECHBM, DipECSRHM (Non-practising) MRCVS
Geraldine Russell BSc, BA
Julie Forrest BVMS, DBR, MRCVS
Elizabeth Burrough, BSc
Alexander CorbishleyMA VetMB PhD FHEA MRSB MRCVS
Abstract
All 107 dairy farmers in South-West Scotland and North-West England belonging to a producer group signed up to a scheme to reduce inhibitory substance (antibiotic) failures. Initial meetings were held in December 2014/January 2015 to discuss the responsible use of medicines, and put forward a 10 point plan for avoiding antibiotic residues in milk. In 2014 (the year prior to the scheme commencing), there were 47 recorded failures in the producer group. This was reduced to 22 failures in 2015, 14 failures in 2016, and 5 failures in the period January to May 2017. The majority of failures were associated with human error such as incorrectly identified cows, accidental transfer of contaminated milk, and cows with poor/inadequate records. Over half the failures involved lactating cow intramammary tubes, and a quarter involved dry cow intramammary tubes.Analysis for potential risk factors showed no significant associations with herd size, BMSCC, Bactoscan, milk yield, number of stockspersons, use of relief milkers, use of internal teat sealants, performing mastitis bacteriology, use of antibiotic testing kits, purchased stock or BVD status.Highlighting practical measures to avoid antibiotic residues entering the bulk tank was sufficient to result in a substantial reduction in recorded failures.
Keywords: antibiotic, failures, milk, cow, residues
Introduction
With the current focus on antimicrobial (especially antibiotic) use in agriculture, reducing levels of inhibitory substance (antibiotic) failuresis not only important for financial and food safety concerns, but also to reduce the risk of antibiotics entering the human food chain and thus the development of antimicrobial resistance.
In 1984-85, 0.4% of bulk tank milk samples failed antibiotic residue tests, which at that time used a sensitivity of 0.02 IU/ml penicillin (Booth 1982, Booth and Harding, 1986; equivalent to 12 µg/l). More recent analysis has shown a failure rate of approximately 0.25% of bulk tank samples analysed by NML in 2013-14 (using DelvotestSP-NT with a sensitivity of 2 µg/l Penicillin G), with a conservative calculation that such failures cost UK dairy farmers and producers approximately £5 million per year in lost milk sales and disposal costs (Hampton, unpublished observations from BCVA Congress 2014).
Summaries of on-farm investigations reported by Booth (1982) showed that the two main reasons for failures were unsatisfactory or lack of record keeping (32% of antibiotic failures), and farmers failing to withhold milk for the full withdrawal period (32% of antibiotic failures). Cows calving early or with a short dry period were responsible for 15% of failures, with accidental transfer of contaminated milk (14%) and prolonged excretion (12%) the next most common reasons. In contrast, a more recent US study quoted by Edmondson (2003) found that employee error (24.6%), unknown (20.1%) and off-label drug use (17.2%) were the most frequent causes of antibiotic failure.
Booth (1982) reported that lactating cow intramammary preparations were responsible for 62% of failures, dry cow intramammary preparations were responsible for 31%, injectable preparations 6%, and other products were responsible for 1%. Booth and Harding (1986) reported similar findings, with the vast majority of failures due to the use of lactating cow (over 50%) and dry cow (25%) intramammary preparations. These findings would highlight the high risk of antibiotic products used for the treatment and prevention of mastitis in antibiotic failures.
Measures taken to avoid antibiotic residues in milk are described in detail by Edmondson (2003) and Edmondson (2007), with a 12 point plan to reduce the potential risk. The issue has been highlighted recently in 2014 with a “Best practices for preventing medicine residues in milk” poster sent to all UK dairy farmers, and the launch of MilkSure in 2016 by DairyUK and the BCVA to “safeguard the production of wholesome milk which is free of veterinary medicine residues” (MilkSure 2016).
Despite these recent developments and the growing public concern about the use of antibiotics in agriculture, there is relatively little recent work published on reducing antibiotic failures, and getting dairy farmers to implement change on their farms for the reduction in failures. This study reports on the activities of a producer group with a higher than average prevalence of antibiotic failures. An active system was set up to investigate all reported antibiotic failures, and farmer workshops were used to highlight “best practice” in reducing the prevalence of antibiotic failures over a 3 year period.
Materials and methods
The producer group consisted of between 100 and 107 dairy farmers based in South-West Scotland and North-West England (numbers varied depending on year, with some producers leaving and/or joining the group). All of the producers in the dedicated supply group signed up to the scheme, and initial farmer meetings were held in December 2014/January 2015 which all farmers attended. The purpose of the initial meeting was to outline the scheme, discuss the responsible use of medicines on farm, and put forward a 10 point plan for avoiding antibiotic residues in milk (based on that proposed by Edmondson 2003).
Prior to this work commencing, all antibiotic failures had been investigated using a telephone call from the milk purchaser to the farmer concerned, and the response was that 80% of failures were of unknown origin. Under the revised scheme, all antibiotic failures were to be reported to DHHPS vets by the milk purchaser on a monthly basis from January 2015 onwards. Farms were then telephoned by the DHHPS vet to investigate the cause of the antibiotic failure, using the BCVA “Investigation of inhibitory substances found in milk” report form as the basis for the investigation.
The results of all investigations were reported back to the milk purchaser, and summaries of the failures and results of the investigations were discussed as part of the annual producer group meetings.Overall the scheme was positively received by the vast majority of the farmers involved. All farmers that were telephoned as part of the inhibitory substance failure investigations appeared to be open and honest in their discussions about the potential causes.
Antibiotic failures could originate from three potential sources: 1) All milk tankers were tested on arrival at the depot using a rapid test (BetaStar Combo [Neogen] which identifies β-lactams and tetracyclines; or Trisensor [Unisensor] with identifies β-lactams,tetracyclines and sulphonamides). 2) Milk samplesfrom all farms were randomly tested once a week via NML using Delvotest SP-NT [DSM] for the presence of inhibitory substances. 3) Farmers reported suspect antibiotic failures to the milk purchaser under the Unmarketable Milk Scheme (UMS), so that the milk was collected separately and did not contaminate other supplies.
Reasons for antibiotic failures were categorised according to previous definitions, based on Edmondson (2003). Information on herd characteristics (numbers of adult cows, lactation milk yield, use of relief milkers etc.) were obtained from a questionnaire survey and consent form distributed at the initial meetings. Bulk tank somatic cell count (BMSCC) and Bactoscan (BSC) data for each herd were obtained via NML for all farms in 2014, prior to the initial farm meetings when the highest incidence of antibiotic failures was reported. Geometric mean BMSCC and BSC were calculated for the whole year using all available figures. The majority of farms were on weekly NML recording, although a proportion had daily NML recordings performed (13 farms had more than 60 NML recordings in 2014), and therefore it was considered that counting the number of individual BMSCC recordings over 400,000 cells/ml was the best measure of capturing outlier herds with BMSCC issues.
All statistical analyses were performed using Minitab 17, using the Odds Ratio function in logistic regression.
Results
In the 12 months prior to the scheme starting, there were 47 recorded antibiotic failures in the producer group in 2014. Data was not available on the breakdown of the failures (ie. if they were tanker failures, NML routine testing or UMS reported failures). However on the assumption that each herd would have been tested weekly by NML, this would represent a failure rate of approximately 0.5% of all samples tested.
As can be seen in Figure 1, the number of recorded antibiotic failures dropped from 47 in 2014, to 22 in 2015, to 14 in 2016, and only 5 recorded antibiotic failures in the period January to May 2017. There was also a distinct seasonal trend in antibiotic failures, with more failures reported in the winter and spring months, compared to summer and autumn periods.
Of the 41 antibiotic fails recorded in 2015 – 2017,31 were detected by routine weekly NML testing, 7 were reported by the farmers under the UMS, and5 were tanker rejections. Note that UMS failures are not current reported to the Food Standards Agency, and so the overall figure in this study is likely to be higher than national UK figures that are reported due to the inclusion of UMS failures.
The majority of farms (78 or 73%) recorded no antibiotic failures during the period 2015-2017. Twenty farms had a single failure, 7 farms had two failures, one farm had three failures, and one farm had four failures during this period.
Table 1 shows that over half of the antibiotic failures were associated with the use of lactating cow intramammary tubes, with a further quarter associated with the use of dry cow intramammary tubes.
Investigations of the reported antibiotic failures were performed using a telephone conversation with the farmer concerned. DHHPS vets did not visit the farm to investigate the reported failure, and there was no subsequent testing of the milk samples for the specific antibiotic that might have caused the failure. As such, the data presented in Table 2 is based on farmer recollection of the incident, and their assumptions as to the cause of the failure. The main reasons provided for antibiotic failures were human error: either incorrectly identified cows, accidental transfer of milk (ie. the cow under treatment was correctly identified, but for some reason her milk was not kept out of the bulk tank), or cows under treatment with no record.
The majority of other reasons for antibiotic failure were relatively infrequent. Only three failures were reported as genuinely unknown, despite prolonged investigation. Of the two “other” categories, one involved the oral administration of Intradine™ (sulphonamide antibiotic) for diarrhoea in an adult milking cow, which the farmer did not realise was an antibiotic preparation given “off-label”. The other was a correctly identified cow under treatment for mastitis that was accidentally milked into the bulk tank, but the farmer was not aware of how this occurred.
Analyses of the potential risk factors for the occurrence of antibiotic failures in 2014 are provided in Table 3. It was decided to perform this analyses for the 2014 data only as this was prior to the intervention with the producer group (ie. before the first farmer meetings in December 2014 and January 2015), and so before antibiotic failures were highlighted as being a significant concern within the group. It was hypothesised that this intervention might potentially bias subsequent data on risk factors for antibiotic failures, given that farmers would have been given information on how to reduce such risks.
The data in Table 3 shows that none of the potential risk factors examined (herd size, BMSCC, BSC, herd size, use of relief milkers etc.) were significantly associated with the occurrence of antibiotic failures in 2014 in the producer group.
Discussion
This work showed a marked reduction in the number of antibiotic failures recorded by the producer group from the baseline year in 2014, with a threefold reduction in antibiotic failures from 2014 to 2016. This positive impact was the result of constructive engagement between the milk purchaser, farmers and veterinary surgeons highlighting the potential issues arising from antibiotic contamination of milk, and the negative effects on product quality and the consumer image of milk.
It is of interest that this reduction was achieved without any active “on farm” intervention on behalf of either the milk purchaser or DHHPS veterinary surgeons, with no additional penalties imposed on the farmers (over and above the “standard” heavy penalties applied in the UK including a 1ppl milk price for the consigned contaminated milk). There were no farm visits arranged, nor increased testing of milk, nor compulsory screening of suspect samples, nor compulsory strict protocols for dealing with treated cows in the parlour. The main methods of engagement were to highlight concerns that the milk purchaser had with antibiotic failures, the lack of feedback in 2014 regarding the potential causes of antibiotic failures, and detail best practice in avoiding antibiotic residues in milk (as detailed by Edmondson 2003). Atkinson (2010) describes the “cycle of change”, and the actual experimentation (or “making it work”) phase that he describes in this model was up to farmers, with no additional motivation provided.
Dutch studies looking at national programmes to improve udder health found that both farmer motivation (in this case economic factors such as increased milk price and reduced losses, especially at a time when milk prices were under pressure) and the overall aim of the campaign (in this case the wider benefit of consumer perception of milk as a clean health product free of contaminants, and the wider issues surrounding the use of antibiotics in agriculture) need to be communicated effectively to farmers (Jansen and others 2010b).This is an example of solution-orientated communication as described by Kleen and others (2011), with the aim of making long-term changes to improve milk quality. Dutch experience was that a combination of communication techniques needed to be adopted to reach all of the farmers (Jansen and others 2000a), and in this case both farmer workshops, telephone calls and information leaflets were all used to highlight the issues involved. Compulsory attendance at producer meetings was thought to be critical so that all farmers understood the importance of the campaign, and the involvement of the producer steering group also facilitated farmer engagement.
Results of the investigations into antibiotic failures outlined in this work are broadly similar to previous reported studies (Booth 1982, Booth and Harding 1986, Edmondson 2003). Table 1 shows that milking cow and dry cow intramammary preparations are responsible for over ¾ of the antibiotic failures in this study, and this would suggest that mastitis control and udder health is a key area to focus on. One route to reducing the risk of antibiotic failures is to reduce the use of antibiotics, and improving udder health would appear critical in this regard.
It is of interest that Booth (1982) reported a marked seasonal pattern to antibiotic failure rates with higher failure rates in the winter, which was also seen in the current study (Figure 1). Exactly why this seasonal trend occurs is not readily apparent. There is generally more farm work during winter with cows to house and feed, and it might be that time pressure adds to potential risks for human error to occur. Alternatively it could be that more environmental mastitis issues occur during the winter housing period, which increases antibiotic use, and thus the risk for antibiotic failures to occur.
Similar to a previous survey(Booth 1982), lack of adequate treatment records, poor cow identification and accidental milking of cows under treatment into the bulk tank remain the main causes of antibiotic failures. Whilst modern technologies such as voluntary/automated milking systems and parlour cow auto-identification can help, no system is fail-safe from human error. It is of interest to note that product-related problems (such as presumed extended excretion of antibiotic past the withhold period) were uncommon, and impossible to definitely diagnose at the time that these investigations were carried out. However the recent introduction of the InfiniPlex (Randox) array system for screening precise antibiotic residues will allow samples that fail screening tests such as the DelvotestSP-NT to be subsequently analysed to determine the precise antibiotic involved. This will allow more forensic qualitative data to determine the cause of the antibiotic failure.
Previous studies have associated an increased risk of antibiotic residues in milk with the use of relief milkers, and a reduced risk associated with the use of on-farm residue testing kits and increased withholding times (McEwen and others 1991). Milk that failed antibiotic residue tests also had a higher BMSCC in a Wisconsin study (Ruegg and Tabone 2000), although one interpretation of this finding is that milk samples from failed samples were likely to be from cows treated for mastitis (as most antibiotic failures are associated with the use of antibiotics to treat mastitis), and so are also more likely to have a higher somatic cell count. This study found no significant risk factors for the occurrence of antibiotic failures in one year of the dataset, although this dataset may have been too small to observe any statistically significant differences. The risk of antibiotic residues getting into milk is a complex process involving human, environmental, cow, product and farm management practices, and many of these interact to result in antibiotic failures.